Nutrient-rich plankton communities stabilized via predator-prey interactions: revisiting the role of vertical heterogeneity.

Self-regulation of population dynamics in nutrient-rich (eutrophic) ecosystems has been a fascinating topic for decades in ecological literature. Simple theoretical models predict population oscillations of large amplitudes in such systems, those predictions often being at odds with reality. Plankton communities possess a particular combination of two important properties, making them unique among ecosystems with eutrophication. These are: (i) the existence of a pronounced spatial gradient of the prey growth rate (through light attenuation with depth) and (ii) the presence of fast-moving predator (zooplankton) capable of quick adjustment of grazing load in vertical direction throughout the whole habitat. Surprisingly, the interplay of those factors is rarely taken into account while analysing stability of nutrient-rich plankton communities. In this paper, we construct generic plankton models (based on integro-differential equations) incorporating the light attenuation in the water column as well as food-searching behaviour of zooplankton. We found that the interplay between the two factors would stabilize a system at low species densities even for an 'unlimited' nutrient stock (infinite system's carrying capacity). Different possible scenarios of stabilization have been found. Since both the vertical gradient of light and the active food search by zooplankton in the column are common characteristics of real plankton communities, we suggest that the obtained mechanism of self-regulation is rather generic in nature. We argue that taking into account this mechanism would be important for understanding the dynamics of nutrient-rich low-chlorophyll ocean systems as well as major causes of non-seasonal plankton blooms.

[1]  P. K. Bjørnsen,et al.  Zooplankton grazing and growth: Scaling within the 2‐2,‐μm body size range , 1997 .

[2]  Christiane Lancelot,et al.  Modeling phytoplankton blooms and carbon export production in the Southern Ocean : dominant controls by light and iron in the Atlantic sector in Austral spring 1992 , 2000 .

[3]  P. Verity,et al.  Abundance and biomass of pico-, namo-, and microplankton on a transact across Nordvestbanken, north Norwegian shelf, in 1994 , 1999 .

[4]  R. Livingston.  Eutrophication Processes in Coastal Systems: Origin and Succession of Plankton Blooms and Effects on Secondary Production in Gulf Coast Estuaries , 2000 .

[5]  T. Smayda,et al.  Complexity in the eutrophication–harmful algal bloom relationship, with comment on the importance of grazing , 2008 .

[6]  Vincent A. A. Jansen,et al.  Regulation of predator-prey systems through spatial interactions:a possible solution to the paradox of enrichment. , 1995 .

[7]  Xabier Irigoien,et al.  Phytoplankton blooms: a ‘loophole’ in microzooplankton grazing impact? , 2005 .

[8]  A. Leising,et al.  Copepod foraging and predation risk within the surface layer during night-time feeding forays , 2005 .

[9]  A. J. Southward,et al.  Plankton and Productivity in the Oceans , 1964 .

[10]  Pierre Auger,et al.  Enrichment Paradox Induced by Spatial Heterogeneity in a Phytoplankton - Zooplankton System , 2008 .

[11]  S. Bollens,et al.  Predator-induced diet vertical migration in a planktonic copepod , 1989 .

[12]  R. Armstrong,et al.  Grazing limitation and nutrient limitation in marine ecosystems: Steady state solutions of an ecosystem model with multiple food chains , 1994 .

[13]  Curtiss O. Davis,et al.  Photosynthetic characteristics and estimated growth rates indicate grazing is the proximate control of primary production in the equatorial Pacific , 1992 .

[14]  Gerd Heber,et al.  Food web complexity and chaotic population dynamics , 2002 .

[15]  Carl J. Walters,et al.  Invulnerable Prey and the Paradox of Enrichment , 1996 .

[16]  M. Hoopes,et al.  Stabilizing effects in spatial parasitoid-host and predator-prey models: a review. , 2004, Theoretical population biology.

[17]  S. Falk‐Petersen,et al.  Influence of spatial heterogeneity on the type of zooplankton functional response: A study based on field observations , 2008 .

[18]  I. Hense,et al.  Beneath the surface: Characteristics of oceanic ecosystems under weak mixing conditions – A theoretical investigation , 2007 .

[19]  A. Cembella,et al.  Toxin accumulation and feeding behaviour of the planktonic copepod Calanus finmarchicus exposed to the red-tide dinoflagellate Alexandrium excavatum , 1995 .

[20]  T. Platt,et al.  Numerical modelling of diel carbon production and zooplankton grazing on the Scotian shelf based on observational data , 1983 .

[21]  Donald M. Anderson,et al.  Toxic Marine Phytoplankton , 1987 .

[22]  K. Tande,et al.  Vertical distributions of primary production and grazing by Calanus glacialis jaschnov and C. hyperboreus krøyer in Arctic waters (Barents Sea) , 1989, Polar Biology.

[23]  Seasonal and spatial changes in easily soluble P in buffer zones under , 2010 .

[24]  Anne-Marie Slaughter,et al.  Grazing impact of mesozooplankton in an upwelling region off northern California, 2000-2003 , 2006 .

[25]  M. Daase,et al.  Vertical distribution of Calanus spp. and Metridia longa at four Arctic locations , 2008 .

[26]  N. Nezlin,et al.  Towards resolving the paradox of enrichment: the impact of zooplankton vertical migrations on plankton systems stability. , 2007, Journal of theoretical biology.

[27]  D. R. Robertson,et al.  Spread of Diadema Mass Mortality Through the Caribbean , 1984, Science.

[28]  R. Arditi,et al.  The effect of a time-delay in a predator-prey model , 1977 .

[29]  B. Manly,et al.  Trade–offs in the vertical distribution of zooplankton: ideal free distribution with costs? , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[30]  Marten Scheffer,et al.  Implications of spatial heterogeneity for the paradox of enrichment , 1995 .

[31]  Robert M. May,et al.  Stability and Complexity in Model Ecosystems , 2019, IEEE Transactions on Systems, Man, and Cybernetics.

[32]  A. M. Edwards,et al.  Zooplankton mortality and the dynamical behaviour of plankton population models , 1999, Bulletin of mathematical biology.

[33]  J. Steele,et al.  The role of predation in plankton models , 1992 .

[34]  M. Rosenzweig.  Paradox of Enrichment: Destabilization of Exploitation Ecosystems in Ecological Time , 1971, Science.

[35]  M E Gilpin,et al.  Enriched predator-prey systems: theoretical stability. , 1972, Science.

[36]  E. Saiz,et al.  Scaling of feeding in marine calanoid copepods , 2007 .

[37]  E. Hansen,et al.  Arctic zooplankton do not perform diel vertical migration (DVM) during periods of midnight sun , 2006 .

[38]  Louis A. Codispoti,et al.  The Role of Eutrophication in the Global Proliferation of Harmful Algal Blooms , 2005 .

[39]  P. Tester,et al.  Toxic marine phytoplankton, zooplankton grazers, and pelagic food webs , 1997 .

[40]  J. Giske,et al.  Ideal free distribution of copepods under predation risk , 1997 .

[41]  Michael R. Landry,et al.  Phytoplankton growth, microzooplankton grazing, and carbon cycling in marine systems , 2004 .

[42]  E. Buskey.  How does eutrophication affect the role of grazers in harmful algal bloom dynamics , 2008 .

[43]  W. Wilson,et al.  Pattern Formation and the Spatial Scale of Interaction between Predators and Their Prey. , 1998, Theoretical population biology.

[44]  K. Banse.  Zooplankton: Pivotal role in the control of ocean production I. Biomass and production , 1995 .

[45]  Mark D. Ohman,et al.  The Demographic Benefits of Diel Vertical Migration by Zooplankton , 1990 .

[46]  Shovonlal Roy,et al.  The stability of ecosystems: A brief overview of the paradox of enrichment , 2007, Journal of Biosciences.

[47]  P. Boyd,et al.  ENVIRONMENTAL FACTORS CONTROLLING PHYTOPLANKTON PROCESSES IN THE SOUTHERN OCEAN1 , 2002 .

[48]  S. Bollens,et al.  Vertical distributions and susceptibilities to vertebrate predation of the marine copepods Metridia lucens and Calanus pacificus , 1993 .

[49]  Francisco P. Chavez,et al.  Phytoplankton taxa in relation to primary production in the equatorial Pacific , 1990 .

[50]  M. Begon,et al.  Ecology: From Individuals to Ecosystems , 2005 .

[51]  James W. Murray,et al.  Functional responses for zooplankton feeding on multiple resources: a review of assumptions and biological dynamics , 2003 .

[52]  K. Banse.  GRAZING AND ZOOPLANKTON PRODUCTION AS KEY CONTROLS OF PHYTOPLANKTON PRODUCTION IN THE OPEN OCEAN , 1994 .

[53]  Timothy J. Cowles,et al.  Grazing patterns of copepods in the upwelling system off Peru , 1980 .

[54]  William W. Murdoch,et al.  Large-amplitude cycles of Daphnia and its algal prey in enriched environments , 1999, Nature.