Abstract
Harmful algal blooms (HABs) characterized by a large concentration of toxic species appear rather rarely, but have a severe impact on the whole ecosystem. To study on possible trigger mechanisms for the emergence of HABs, we consider a nutrient-phytoplankton-zooplankton model to find the conditions under which a toxic phytoplankton species is able to form a bloom by winning the competition against its nontoxic competitor. The basic mechanism is related to the excitability of the system, i.e., the ability to develop a large response on certain perturbations. In a large class of models, a HAB results from a combined effect of nutrient enrichment and selective predation on different phytoplankton populations by zooplankton. We show that the severity of HAB is controlled by nutrient enrichment and zooplankton abundance, while the frequency of its occurrence depends on the strength of selectivity of predation. Thereby the intricate interplay between excitability, competition, and selective grazing pressure builds the backbone of the mechanism of the emergence of HABs.
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References
Anderson DM (2003) The expanding global problem of harmful algal blooms. In: Ragaini R (ed) International seminar on nuclear war and planetary emergencies, 27th session, Erice, Italy, 18–26 August 2002. World Scientific Publishing Co., Pte Ltd., Singapore, pp 372–393
Anderson DM (2007) The ecology and oceanography of harmful algal blooms: multidisciplinary approaches to research and management. IOC Bruun memorial lecture. UNESCO, Paris
Anderson CR, Kudela RM, Benitez-Nelson C, Sekula-Wood E, Burrell CT, Chao Y, Langlois G, Goodman J, Siegel DA (2011) Detecting toxic diatom blooms from ocean color and a regional ocean model. Geophys Res Lett 38:L04603
Anderson DM, Cembella AD, Hallegraeff GM (2012) Progress in understanding harmful algal blooms: paradigm shifts and new technologies for research, monitoring, and management. Annu Rev Mar Sci 4:143–176
Banerjee M, Venturino E (2011) A phytoplankton-toxic phytoplankton-zooplankton model. Ecol Complex 8:239–248
Benincà E, Dakos V, van Nes EH, Huisman J, Scheffer M (2011) Resonance of plankton communities with temperature fluctuations. Am Nat 178:E85–E95
Carey CC, Ibelings BW, Hoffmann EP, Hamilton DP, Brookes JD (2012) Eco-physiological adaptations that favour freshwater cyanobacteria in a changing climate. Water Res 46:1394–1407
Caron DA, Gobler CJ, Lonsdale DJ, Buck NJ, Cerrato RM, Schaffner RA, Rose JM, Taylor GT, Boissonneault KR, Mehran R (2004) Microbial herbivory on the brown tide alga, Aureococcus anophagefferens: results from natural ecosystems, mesocosms and laboratory experiments. Harmful Algae 3:439–457
Caron DA, Hutchins DA (2013) The effects of changing climate on microzooplankton grazing and community structure: drivers, predictions and knowledge gaps. J Plank Res 35:235–252
Chakraborty S, Chatterjee S, Venturino E, Chattopadhyay J (2007) Recurring plankton bloom dynamics modeled via toxin producing phytoplankton. J Biol Phys 33:271–290
Chakraborty S, Bhattacharya S, Feudel U, Chattopadhyay J (2012) The role of avoidance by zooplankton for survival and dominance of toxic phytoplankton. Ecol Complex 11:144–153
Clother DR, Brindley J (1999) Excitabilty of an age-structured plankton ecosystem. J Math Biol 39:377–420
DeMott WR, Zhang Q, Carmichael WW (1991) Effects of toxic cyanobacteria and purified toxins on the survival and feeding of a copepod and three species of Daphnia. Limnol Oceanogr 36:1346–1357
Ebenhoh W, Kohlmier C, Radford PJ (1995) The benthic biological submodel in the European regional Seas Ecosystem Model. Neth J Sea Res 33:423–452
Edwards AM, Brindley J (1996) Oscillatory behaviour in a three-component plankton population model. Dyn Stab Syst 11:347–370
Edwards AM, Brindley J (1999) Zooplankton mortality and the dynamical behaviour of plankton population models. Bull Math Biol 61:303–339
Edwards AM (2001) Adding detritus to a nutrient-phytoplankton-zooplankton model: a dynamical-systems approach. J Plank Res 23:389–413
Fasham MJR, Ducklow HW, McKelvie SM (1990) A nitrogen-based model of plankton dynamics in the oceanic mixed layer. J Mar Res 48:591–639
Falkowski PG, Fenchel T, Delong EF (2008) The microbial engines that drive Earth’s biogeochemical cycles. Sci 320:1034–1039
Field CB, Behrenfeld MJ, Randerson JT, Falkowski PG (1998) Primary production of the biosphere: integrating terrestrial and oceanic components. Sci 281:237–240
Flynn KJ (2008) Attack is not the best form for defence: lessons from harmful algal bloom dynamics. Harmful Algae 8:129–139
Franks PJS (1997) Spatial patterns in dense algal blooms. Limnol Oceanogr 42:1297–1305
Freund JA, Mieruch S, Scholze B, Wiltshire K, Fleude U (2006) Bloom dynamics in a seasonally forced phytoplankton-zooplankton model: trigger mechanisms and timing effects. Ecol Complex 3:129–139
Frost BW (1972) Effects of size and concentration of food particles on the feeding behavior of the marine planktonic copepod Calanus pacificus. Limnol Oceanogr 17:805–815
Gentleman W, Leising A, Frost B, Strom S, Murray J (2003) Functional responses for zooplankton feeding on multiple resources: a critical review of assumed biological dynamics. Deep-Sea Res II(50):2847–2875
Glibert PM, Allen JI, Bouwman AF, Brown CW, Flynn KJ, Lewitus AJ, Madden CJ (2010) Modeling of HABs and eutrophication status, advances, challenges. J Mar Syst 83:262–275
Gobler CJ, Sunda WG (2012) Ecosystem disruptive algal blooms of the brown tide species, Aureococcus anophagefferens and Aureoumbra lagunensis. Harmful Algae 14:36–45
Grover JP, Crane KW, Baker JW, Brooks BW, Roelke DL (2011) Spatial variation of harmful algae and their toxins in flowing-water habitats: a theoretical exploration. J Plank Res 33:211–227
Grover JP, Roelkeb DL, Brooks BW (2012) Modeling of plankton community dynamics characterized by algal toxicity and allelopathy: a focus on historical Prymnesium parvum blooms in a Texas reservoir. Ecol Model 227:147–161
Hallegraeff GM (1993) A review of harmful algal blooms and their apparent global increase. Phycologia 32:79–99
Harvey EL, Menden-Deuer S (2012) Predator-induced fleeing behaviors in phytoplankton: a new mechanism for harmful algal bloom formation Plos One e46438:7
Huang DW, Wang HL, Feng JF, Zhu ZW (2008) Modelling algal densities in harmful algal blooms (HAB) with stochastic dynamics. Appl Math Model 32:1318–1326
Hulot FD, Huisman J (2004) Allelopathic interactions between phytoplankton species: the roles of heterotrophic bacteria and mixing intensity. Limnol Oceanogr 49:1424–1434
Huntley M, Sykes P, Rohan S, Martin V (1986) Chemically-mediated rejection of dinoflagellate prey by the copepods Calanus pacificus and Paracalanus parvus: mechanism, occurrence and significance. Mar Ecol Prog Ser 28:105–120
Huppert A, Olinky R, Stone L (2004) Bottom-up excitable models of phytoplankton blooms. Bull Math Biol 66:865–878
Izhikevich EM (2000) Neural excitability, spiking, and bursting. Int J Bifurcation Chaos 10:1171–1266
Izhikevich EM (2007) Dynamical systems in neuroscience: the geometry of excitability and bursting. MIT, Cambridge, pp 325–378
Kim HG (2010) An Overview on the occurrences of harmful algal blooms (HABs) and mitigation strategies in Korean coastal waters. In: Ishimatsu A, Lie H-J (eds) Coastal environmental and ecosystem issues of the East China Sea. TERRAPUB, Tokyo, pp 121–131
Kurmayer R, Juttner F (1999) Strategies for the co-existence of zooplankton with the toxic cyanobacterium Planktothrix rubescens in Lake Zurich. J Plank Res 21:659–683
Lampert W (1982) Further studies on the inhibitory effect of toxic bluegreen Microcystis aeruginosu on the filtering rate of zooplankton. Arch Hydrobiol 95:207–220
Llebot C, Spitz YH, Solé J, Estrada M (2010) The role of inorganic nutrients and dissolved organic phosphorus in the phytoplankton dynamics of a Mediterranean Bay: a modeling study. J Mar Syst 83:192–209
Lohmann G, Wiltshire KH (2012) Winter atmospheric circulation signature for the timing of the spring bloom of diatoms in the North Sea. Mar Biol 159:2573–2581
Lonsdale DJ, Cosper EM, Kim WS, Doall MH, Divadeenam A, Jonasdottir SH (1996) Food web interactions in the plankton of Long Island bays, with preliminary observations on brown tide effects. Mar Ecol Prog Ser 134:247–263
Machado PA (1979) Dinoflagellate bloom on the Brazilian South Atlantic coast. In: Taylor DL, Seliger HH (eds) Toxic dinoflagellate blooms. Elsevier, New York, pp 29–32
Makarewicz JC, Lewis TW, Bertram P (1999) Phytoplankton composition and biomass in the offshore waters of Lake Erie: pre-and post-Dreissena introduction (1983–1993). J Great Lakes Res 25:135–148
McGillicuddy DJ (2010) Models of harmful algal blooms: conceptual, empirical, and numerical approaches. J Mar Syst 83:105–107
Nehring S (1993) Mechanisms for recurrent nuisance algal blooms in coastal zones: resting cyst formation as life-strategy of dinoflagellates. In: Sterr H, Hofstade J, Plag HP (eds) Proc Int Coastal Congr, ICC-Kiel, 1992. Peter Lang, Frankfurt, pp 454–467
Pal S, Chatterjee S, Das K, Chattopadhyay J (2009) Role of competition in phytoplankton population for the occurrence and control of plankton bloom in the presence of environmental fluctuations. Ecol Model 220:96–110
Pitchford JW (1997) Dynamics of multi-species plankton populations, PhD thesis, University of Leeds
Pitchford JW, Brindley J (1999) Iron limitation, grazing pressure and oceanic high nutrient-low chlorophyll (HNLC) regions. J Plank Res 21:525–547
Scheffer M, Rinaldi S, Kuznetsov YA, Van Nes EH (1997) Seasonal dynamics of Daphnia and algae explained as a periodically forced predator-prey system. Oikos 80:519–532
Schultz M, Kiørboe T (2009) Active prey selection in two pelagic copepods feeding on potentially toxic and non-toxic dinoflagellates. J Plankt Res 31:553–561
Solé J, Garcia-Ladona E, Estrada M (2006) The role of selective predation in harmful algal blooms. J Mar Syst 62:46–54
Steele JH, Henderson EW (1981) A simple plankton model. Am Nat 117:676–691
Sunda WG, Shertzer KW (2012) Modeling ecosystem disruptive algal blooms: positive feedback mechanisms. Mar Ecol Prog Ser 447:31–47
Teegarden GJ (1999) Copepod grazing selection and particle discrimination on the basis of PSP toxin content. Marine Ecology Progress Series 181:163–176
Teramoto E, Kawasaki K, Shigesada N (1979) Switching effect of predation on competitive prey species. J Theor Biol 79:303–315
Truscott JE, Brindley J (1994a) Ocean plankton populations as excitable media. Bull Math Biol 56:981–998
Truscott JE, Brindley J (1994b) Equilibria, stability and excitability in a general class of plankton population-models. Philos Trans R Soc Lond A 347:703–718
Uye S, Takamatsu K (1990) Feeding interactions between planktonic copepods and red-tide flagellates from Japanese costal waters. Mar Ecol Prog Ser 59:97–107
Vanderploeg HA, Liebig JR, Carmichael WW, Agy MA, Johengen TH, Fahnenstiel GL, Nalepa TF (2001) Zebra mussel (Dreissena polymorpha) selective filtration promoted toxic Microcystis blooms in Saginaw Bay (Lake Huron) and Lake Erie. Can J Fish Aquat Sci 58:1208–1221
Wang XD, Qin BQ, Gao G, Paerl HW (2010) Nutrient enrichment and selective predation by zooplankton promote Microcystis (Cyanobacteria) bloom formation. J Plankton Res 32:457–470
Wyatt T, Horwood J (1973) Model which generates red tides Nature 244:238–240
Yoshiyama K, Mellard JP, Litchman E, Klausmeier CA (2009) Phytoplankton competition for nutrients and light in a stratified water column. Am Nat 174:190–203
Acknowledgments
The authors wish to thank Michaela Busch, Dave Caron, Helmut Hillebrand, and Stefanie Moorthi for valuable discussions. Furthermore, the authors would like to thank an unknown reviewer for pointing out a very interesting paper on zooplankton dynamics, which led to the analysis of the second model. S.C. thanks the Alexander von Humboldt Foundation for financial support in the form of a postdoctoral fellowship. U.F. thanks R. Roy and his group for their hospitality and the Burgers Program for Fluid Dynamics of the University of Maryland at College Park for financial support. U.F. acknowledges support from the Volkswagen-Foundation, Grant No. 85388.
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Chakraborty, S., Feudel, U. Harmful algal blooms: combining excitability and competition. Theor Ecol 7, 221–237 (2014). https://doi.org/10.1007/s12080-014-0212-1
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DOI: https://doi.org/10.1007/s12080-014-0212-1