Analysis of self-overlap reveals trade-offs in plankton swimming trajectories

Movement is a fundamental behaviour of organisms that not only brings about beneficial encounters with resources and mates, but also at the same time exposes the organism to dangerous encounters with predators. The movement patterns adopted by organisms should reflect a balance between these contrasting processes. This trade-off can be hypothesized as being evident in the behaviour of plankton, which inhabit a dilute three-dimensional environment with few refuges or orienting landmarks. We present an analysis of the swimming path geometries based on a volumetric Monte Carlo sampling approach, which is particularly adept at revealing such trade-offs by measuring the self-overlap of the trajectories. Application of this method to experimentally measured trajectories reveals that swimming patterns in copepods are shaped to efficiently explore volumes at small scales, while achieving a large overlap at larger scales. Regularities in the observed trajectories make the transition between these two regimes always sharper than in randomized trajectories or as predicted by random walk theory. Thus, real trajectories present a stronger separation between exploration for food and exposure to predators. The specific scale and features of this transition depend on species, gender and local environmental conditions, pointing at adaptation to state and stage-dependent evolutionary trade-offs.

[1]  Pawel Romanczuk,et al.  Nutritional state and collective motion: from individuals to mass migration , 2011, Proceedings of the Royal Society B: Biological Sciences.

[2]  J. Videler,et al.  Copepod feeding currents: flow patterns, filtration rates and energetics , 2003, Journal of Experimental Biology.

[3]  L. Dubroca,et al.  Unexpected Regularity in Swimming Behavior of Clausocalanus furcatus Revealed by a Telecentric 3D Computer Vision System , 2013, PloS one.

[4]  Simone Pigolotti,et al.  Correction: ‘Analysis of self-overlap reveals trade-offs in plankton swimming trajectories’ , 2014, Journal of The Royal Society Interface.

[5]  G. Paffenhöfer,et al.  Prey capture in Clausocalanus furcatus (Copepoda: Calanoida). The role of swimming behaviour , 2008 .

[6]  Kurt Binder,et al.  Monte Carlo Simulation in Statistical Physics , 1992, Graduate Texts in Physics.

[7]  George Kehayias,et al.  The diets of the chaetognaths Sagitta enflata, S. serratodentata atlantica and S. bipunctata at different seasons in Eastern Mediterranean coastal waters , 1996 .

[8]  E. Zambianchi,et al.  Lagrangian modelling of swimming behaviour and encounter success in co-occurring copepods: Clausocalanus furcatus vs. Oithona plumifera , 2010 .

[9]  Sidney Redner,et al.  A guide to first-passage processes , 2001 .

[10]  Sean P. Colin,et al.  Locating a mate in 3D: the case of Temora longicornis , 1998 .

[11]  Kurt Binder,et al.  Monte Carlo Simulation in Statistical Physics , 1992, Graduate Texts in Physics.

[12]  T. Fenchel,et al.  The functional biology of Strombidium sulcatum, a marine oligotrich ciliate (Ciliophora, Oligotrichida) , 1988 .

[13]  John J. Videler,et al.  Escape from viscosity: the kinematics and hydrodynamics of copepod foraging and escape swimming , 2003, Journal of Experimental Biology.

[14]  I. Couzin,et al.  Effective leadership and decision-making in animal groups on the move , 2005, Nature.

[15]  Laurent Seuront,et al.  Multifractal random walk in copepod behavior , 2001 .

[16]  J. Klafter,et al.  Feeding and Swimming Behavior in Grazing Microzooplankton1,2 , 1988 .

[17]  H. Berg Random Walks in Biology , 2018 .

[18]  J. Yen,et al.  Quantifying copepod kinematics in a laboratory turbulence apparatus , 2008 .

[19]  Peter A. Thompson,et al.  A Mechanistic Approach to Plankton Ecology , 2012 .

[20]  Olga Mangoni,et al.  Seasonal patterns in plankton communities in a pluriannual time series at a coastal Mediterranean site (Gulf of Naples): an attempt to discern recurrences and trends , 2004 .

[21]  P. A. Prince,et al.  Lévy flight search patterns of wandering albatrosses , 1996, Nature.

[22]  F. Spaccesi Abundance, recruitment, and shell growth of the exotic mussel Limnoperna fortunei in the Río de la Plata (Argentina) , 2013, Zoological Studies.

[23]  Edward J. Buskey,et al.  Copepod escape behavior in non-turbulent and turbulent hydrodynamic regimes , 2007 .

[24]  Jiang‐Shiou Hwang,et al.  The different aspects in motion of the three reproductive stages of Pseudodiaptomus annandalei (Copepoda, Calanoida) , 2010 .

[25]  S. Redner A guide to first-passage processes , 2001 .

[26]  S. Harris Steady absorption of Brownian particles by a sphere , 1982 .

[27]  Ran Nathan,et al.  An emerging movement ecology paradigm , 2008, Proceedings of the National Academy of Sciences.

[28]  J. Titelman,et al.  Swimming and escape behavior of copepod nauplii: implications for predator-prey interactions among copepods , 2001 .

[29]  J. Gerritsen,et al.  Encounter Probabilities and Community Structure in Zooplankton: a Mathematical Model , 1977 .

[30]  L. Dubroca,et al.  Zooplankton associations in a Mediterranean long-term time-series , 2011 .

[31]  E. Zambianchi,et al.  Behaviour-dependent predation risk in swimming zooplankters , 2013, Zoological Studies.

[32]  T. Kiørboe Optimal swimming strategies in mate-searching pelagic copepods , 2008, Oecologia.

[33]  André W. Visser,et al.  Motility of zooplankton: fitness, foraging and predation , 2007 .

[34]  F. Bartumeus,et al.  Helical Lévy walks: Adjusting searching statistics to resource availability in microzooplankton , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Simon Benhamou,et al.  How many animals really do the Lévy walk? , 2008, Ecology.

[36]  G. Paffenhöfer,et al.  From small scales to the big picture: persistence mechanisms of planktonic grazers in the oligotrophic ocean , 2007 .

[37]  André W. Visser,et al.  Plankton motility patterns and encounter rates , 2006, Oecologia.

[38]  E. Buskey Swimming pattern as an indicator of the roles of copepod sensory systems in the recognition of food , 1984 .

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