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Chemical contamination-mediated regime shifts in planktonic systems

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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.

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References

  • Banerjee S, Sarkar RR, Chattopadhyay J (2019) Effect of copper contamination on zooplankton epidemics. J Theor Biol 469:61–74

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Beisner BE, Haydon DT, Cuddington K (2003) Alternative stable states in ecology. Front Ecol Environ 1(7):376–382

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Bossuyt BT, Janssen CR (2003) Acclimation of Daphnia magna to environmentally realistic copper concentrations. Comp Biochem Physiol C Toxicol Pharmacol 136:253–264

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Carpenter SR (2005) Eutrophication of aquatic ecosystems: bistability and soil phosphorus. Proc Natl Acad Sci USA 102(29):10002–10005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carpenter SR (2008) Phosphorus control is critical to mitigating eutrophication. Proc Natl Acad Sci USA 105(32):11039–11040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Drake JM (2013) Early warning signals of stochastic switching. Proc Roy Soc B: Biol Sci 280(1766):20130686

    Article  Google Scholar 

  • Evans SN, Ralph PL, Schreiber SJ, Sen A (2013) Stochastic population growth in spatially heterogeneous environments. J Math Biol 66(3):423–476

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Flemming C, Trevors J (1989) Copper toxicity and chemistry in the environment: a review. Water Air Soil Pollut 44(1–2):143–158

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Gutierrez MF, Paggi JC, Gagneten AM (2012) Microcrustaceans escape behavior as an early bioindicator of copper, chromium and endosulfan toxicity. Ecotoxicology 21:428–438

    Article  CAS  PubMed  Google Scholar 

  • Guttal V, Jayaprakash C (2007) Impact of noise on bistable ecological systems. Ecol Model 201(3–4):420–428

    Article  Google Scholar 

  • Halley JM (1996) Ecology, evolution and 1f-noise. Trends Ecol Evol 11(1):33–37

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Havens KE (1994) Structural and functional responses of a freshwater plankton community to acute copper stress. Environ Pollut 86:259–266

    Article  CAS  PubMed  Google Scholar 

  • Higham DJ (2001) An algorithmic introduction to numerical simulation of stochastic differential equations. SIAM Rev 43(3):525–546

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Huang Q, Wang H, Lewis MA (2015) The impact of environmental toxins on predator-prey dynamics. J Theor Biol 378:12–30

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Koivisto S, Ketola M, Walls M (1992) Comparison of five cladoceran species in short-and long-term copper exposure. Hydrobiologia 248:125–136

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Luoma SN, Rainbow PS (2005) Why is metal bioaccumulation so variable? biodynamics as a unifying concept. Environ Sci Technol 39:1921–1931

    Article  CAS  PubMed  Google Scholar 

  • McQueen D, Post J (1988) Cascading trophic interactions: Uncoupling at the zooplankton-phytoplankton link. Hydrobiologia 159(3):277–296

    Article  Google Scholar 

  • Mertz W (1981) The essential trace elements. Science 213:1332–1338

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • O’Keefe TC, Brewer MC, Dodson SI (1998) Swimming behavior of Daphnia: its role in determining predation risk. J Plankton Res 20:973–984

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Prosnier L, Loreau M, Hulot FD (2015) Modeling the direct and indirect effects of copper on phytoplankton zooplankton interactions. Aquat Toxicol 162:73–81

    Article  CAS  PubMed  Google Scholar 

  • Real LA (1977) The kinetics of functional response. Am Nat 111(978):289–300

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Rip J, McCann K (2011) Cross-ecosystem differences in stability and the principle of energy flux. Ecol Lett 14(8):733–740

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Scheffer M, Carpenter S, Foley JA, Folke C, Walker B (2001) Catastrophic shifts in ecosystems. Nature 413(6856):591–596

    Article  CAS  PubMed  Google Scholar 

  • Scheffer M, Carpenter SR (2003) Catastrophic regime shifts in ecosystems: linking theory to observation. Trends Ecol Evol 18(12):648–656

    Article  Google Scholar 

  • Scheffer M, De Boer RJ (1995) Implications of spatial heterogeneity for the paradox of enrichment. Ecology 76(7):2270–2277

    Article  Google Scholar 

  • Scheffer M, Hosper S, Meijer M, Moss B, Jeppesen E (1993) Alternative equilibria in shallow lakes. Trends Ecol Evol 8(8):275–279

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Sekerci Y, Petrovskii S (2015a) Mathematical modelling of plankton-oxygen dynamics under the climate change. Bull Math Biol 77(12):2325–2353

    Article  CAS  PubMed  Google Scholar 

  • Sekerci Y, Petrovskii S (2015b) Mathematical modelling of spatiotemporal dynamics of oxygen in a plankton system. Math Model Nat Phenom 10(2):96–114

    Article  Google Scholar 

  • Sharma Y, Abbott KC, Dutta PS, Gupta A (2015) Stochasticity and bistability in insect outbreak dynamics. Theor Ecol 8(2):163–174

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Yan H, Pan G (2002) Toxicity and bioaccumulation of copper in three green microalgal species. Chemosphere 49:471–476

    Article  CAS  PubMed  Google Scholar 

Download references

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.

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Authors

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

Correspondence to Swarnendu Banerjee.

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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

Fig. 9
figure 9

Probability density estimates of the (A, B, C) phytoplankton and (D, E, F) zooplankton populations under three different external copper concentrations: 5.085 \(\mu g L^{-1}\), 5.095 \(\mu g L^{-1}\) and 5.1 \(\mu g L^{-1}\); \(K=2\) \(mgCL^{-1}\)

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.

Fig. 10
figure 10

Basin of attraction for the bistable scenario for different carrying capacities. Left panel: \(K=2\), \(E=14.3\) \(\mu g L^{-1}\); Right panel: \(K=3\), \(E=16\) \(\mu g L^{-1}\). The red and the blue points denote initial conditions for which the system converges to the zooplankton-dominated and phytoplankton-dominated equilibrium respectively

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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

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