An automated multi-flume actograph for the study of behavioral rhythms of burrowing organisms

Abstract In this study, we present and test the functioning of a automated multi-flume actograph that is able to simulate concomitant geophysical cycles (day-night and hydrodynamic cycles) characterizing the benthic environment of continental margins. The burrowing Norway lobster ( Nephrops norvegicus , L.) was used to test the functioning of the device. The system is endowed with pumps and a pipe system for periodical current flow generation. Monochromatic blue light cycle (472 nm) was provided by submergible LED's lighting strips. Locomotor activity of 8 individuals was tracked by 4 HD video cameras during a 10 days trial. A customized automated video-imaging protocol in MATLAB calculated displacement of animals (cm/min). The functioning of the system was tested simulating an Atlantic continental shelf scenario (i.e. light intensity of 4 · 10 − 3  μE/m 2 /s and current flow at 10 cm/s). Robust time series outputs of nocturnal phase were reported, with the first laboratory evidence of the influence of current flow on burrow emergence of the species. Water flow increase inhibited lobster movement generating a dual reaction in relation to their burrow emergence phase. The method presented here could be pivotal to study unknown aspects of Norway lobster ecology.

[1]  K. Wiese,et al.  Laboratory-based observations of behaviour in Northern krill (Meganyctiphanes norvegica Sars). , 2010, Advances in marine biology.

[2]  W. Watson,et al.  Daily and circadian rhythms of locomotor activity in the American lobster, Homarus americanus , 2005 .

[3]  T Roenneberg,et al.  Twilight Times: Light and the Circadian System , 1997, Photochemistry and photobiology.

[4]  Elizabeth Cook,et al.  Changing coasts: marine aliens and artificial structures , 2012 .

[5]  H. Dircksen,et al.  Circadian clocks in crustaceans: identified neuronal and cellular systems. , 2010, Frontiers in bioscience.

[6]  A. R. Nowell,et al.  FLUMES : THEORETICAL AND EXPERIMENTAL CONSIDERATIONS FOR SIMULATION OF BENTHIC ENVIRONMENTS* , 1987 .

[7]  Paolo Menesatti,et al.  A Novel Morphometry-Based Protocol of Automated Video-Image Analysis for Species Recognition and Activity Rhythms Monitoring in Deep-Sea Fauna , 2009, Sensors.

[8]  Magnus L. Johnson,et al.  Spectral sensitivities of five marine decapod crustaceans and a review of spectral sensitivity variation in relation to habitat , 2002, Journal of the Marine Biological Association of the United Kingdom.

[9]  J. Aguzzi,et al.  Hydrodynamic, non-photic modulation of biorhythms in the Norway lobster, Nephrops norvegicus (L.) , 2009 .

[10]  K. F. Bowden,et al.  Physics of the Sea , 1973, Nature.

[11]  M. Bell,et al.  Trawl catch composition in relation to Norway lobster (Nephrops norvegicus L.) abundance on the Farn Deeps grounds, NE England , 2008 .

[12]  V. Sbragaglia,et al.  Dusk but not dawn burrow emergence rhythms of Nephrops norvegicus (Crustacea: Decapoda) , 2013 .

[13]  E. Naylor,et al.  A combined tidal simulator and actograph for marine animals , 1989 .

[14]  E. Naylor,et al.  Chronobiology: implications for marine resource exploitation and management , 2005 .

[15]  E. Naylor,et al.  Entrainment of the locomotor rhythm of Carcinus by cycles of salinity change , 1977, Journal of the Marine Biological Association of the United Kingdom.

[16]  W. Watson,et al.  Rhythms of Locomotion Expressed by Limulus polyphemus, the American Horseshoe Crab: I. Synchronization by Artificial Tides , 2008, The Biological Bulletin.

[17]  Jacopo Aguzzi,et al.  Light Intensity Determines Temporal Niche Switching of Behavioral Activity in Deep-Water Nephrops norvegicus (Crustacea: Decapoda) , 2010, Journal of biological rhythms.

[18]  R. Atkinson,et al.  Pressure and the rhythmic behaviour of inshore marine animals. , 1972, Symposia of the Society for Experimental Biology.

[19]  M. B. Wiley,et al.  Fine-scale patterns of odor encounter by the antennules of mantis shrimp tracking turbulent plumes in wave-affected and unidirectional flow , 2003, Journal of Experimental Biology.

[20]  E. Naylor,et al.  Chronobiology of Marine Organisms , 2010 .

[21]  Jacopo Aguzzi,et al.  Chronobiology of deep-water decapod crustaceans on continental margins. , 2010, Advances in marine biology.

[22]  Paolo Menesatti,et al.  A New Laboratory Radio Frequency Identification (RFID) System for Behavioural Tracking of Marine Organisms , 2011, Sensors.

[23]  Paolo Menesatti,et al.  Monochromatic blue light entrains diel activity cycles in the Norway lobster, Nephrops norvegicus (L.) as measured by automated video-image analysis , 2009 .

[24]  L. A. Klapow Natural and artificial rephasing of a tidal rhythm , 1972, Journal of comparative physiology.

[25]  Paolo Menesatti,et al.  Behavioral rhythms of hydrocarbon seep fauna in relation to internal tides , 2010 .

[26]  Ming-Shing Young,et al.  Integrated digital image and accelerometer measurements of rat locomotor and vibratory behaviour , 2007, Journal of Neuroscience Methods.

[27]  J. Palmer The biological rhythms and clocks of intertidal animals , 1995 .

[28]  Jacopo Aguzzi,et al.  A new tracking system for the measurement of diel locomotor rhythms in the Norway lobster, Nephrops norvegicus (L.) , 2008, Journal of Neuroscience Methods.

[29]  P. Sokolove,et al.  The chi square periodogram: its utility for analysis of circadian rhythms. , 1978, Journal of theoretical biology.

[30]  E. Naylor Tidal and Diurnal Rhythms of Locomotory Activity in Carcinus Maenas (L.) , 1958 .

[31]  C. Pittendrigh,et al.  Circadian rhythms and the circadian organization of living systems. , 1960, Cold Spring Harbor symposia on quantitative biology.

[32]  E. Naylor,et al.  Synchronization of the Locomotor Tidal Rhythm of Carcinus , 1969 .

[33]  Stepán Obdrzálek,et al.  Object Recognition using Local Affine Frames on Distinguished Regions , 2002, BMVC.

[34]  Jacopo Aguzzi,et al.  A history of recent advancements on Nephrops norvegicus behavioral and physiological rhythms , 2008, Reviews in Fish Biology and Fisheries.

[35]  Edward Gaten,et al.  Depth related variation in the structure and functioning of the compound eye of the Norway lobster Nephrops norvegicus , 1990, Journal of the Marine Biological Association of the United Kingdom.

[36]  Miguel,et al.  CIRCADIAN LOCOMOTOR ACTIVITY AND ITS ENTRAINMENT BY FOOD IN THE CRAYFISH PROCAMBARUS CLARKI , 1994, The Journal of experimental biology.

[37]  P. Puig,et al.  Deep slope currents and suspended particle fluxes in and around the Foix submarine canyon (NW Mediterranean) , 2000 .

[38]  A. L. Rice,et al.  Observations on the burrows and burrowing behaviour of two mud-dwelling decapod crustaceans, Nephrops norvegicus and Goneplax rhomboides , 1971 .

[39]  J. Aschoff,et al.  Exogenous and endogenous components in circadian rhythms. , 1960, Cold Spring Harbor symposia on quantitative biology.

[40]  E. Gaten Light‐induced damage to the dioptric apparatus of nephrops norvegicus (L.) and the quantitative assessment of the damage , 1988 .

[41]  V. Trenkel,et al.  Variability in natural behaviour, and observed reactions to an ROV, by mid-slope fish species , 2006 .

[42]  André Morel,et al.  Relation between total quanta and total energy for aquatic photosynthesis1 , 1974 .

[43]  E. Naylor,et al.  Environmental entrainment of tidally rhythmic behaviour in marine animals , 1984 .

[44]  D. Armstrong,et al.  Swimming behavior of Dungeness crab,Cancer magister Dana, megalopae in still and moving water , 1994 .

[45]  Paolo Menesatti,et al.  Activity rhythms in the deep-sea: a chronobiological approach. , 2011, Frontiers in bioscience.

[46]  J. T. Enright Entrainment of a Tidal Rhythm , 1965, Science.

[47]  H. Aréchiga,et al.  The eye and some effects of light on locomotor activity in Nephrops norvegicus , 1975 .

[48]  T. Breithaupt Chemical Communication in Crayfish , 2010 .

[49]  B. Phillips Lobsters: Biology, Management, Aquaculture and Fisheries , 2013 .

[50]  G. Tarling,et al.  Influence of individual state on swimming capacity and behaviour of Antarctic krill Euphausia superba , 2008 .

[51]  Imants G. Priede,et al.  Rhythms at the bottom of the deep sea : Cyclic current flow changes and melatonin patterns in two species of demersal fish , 2007 .

[52]  R. Orth,et al.  Swimming velocities and behavior of blue crab (Callinectes sapidus rathbun) megalopae in still and flowing water , 1992 .

[53]  J. Basil,et al.  Crayfish (Cherax destructor) use Tactile Cues to Detect and Learn Topographical Changes in Their Environment , 2000 .

[54]  E. Naylor,et al.  Effects of dusk and dawn on locomotor activity rhythms in the norway lobster Nephrops norvegicus , 1977 .

[55]  S. G. Reebs Plasticity of diel and circadian activity rhythms in fishes , 2002, Reviews in Fish Biology and Fisheries.

[56]  Chris Garrett,et al.  Internal Tides and Ocean Mixing , 2003, Science.

[57]  H. Aréchigá,et al.  Distributed Circadian Rhythmicity In The Crustacean Nervous System , 2002 .

[58]  R. Refinetti Non-stationary time series and the robustness of circadian rhythms. , 2004, Journal of theoretical biology.

[59]  P. Snelgrove,et al.  Near-bottom hydrodynamic effects on postlarval settlement in the American lobster Homarus americanus , 2010 .

[60]  M. H. Hastings The entraining effect of turbulence on the circa-tidal activity rhythm and its semi-lunar modulation in Eurydice pulchra , 1981, Journal of the Marine Biological Association of the United Kingdom.

[61]  Douglas M. Neil,et al.  The reactions of the Norway lobster, Nephrops norvegicus (L.), to water currents , 1988 .

[62]  Frank W. Grasso,et al.  Crayfish Inspired Representation of Space via Haptic Memory in a Simulated Robotic Agent , 2012, Living Machines.

[63]  G. P. Ennis Swimming Ability of Larval American Lobsters, Homarus americanus, in Flowing Water , 1986 .

[64]  D. Jones,et al.  The swimming rhythm of the sand beach isopod Eurydice pulchra , 1970 .

[65]  Behavior of the burrowing shrimp Alpheus macellarius in varying gravel substrate conditions , 2005, Journal of Ethology.

[66]  Jacopo Aguzzi,et al.  Sensory biology and behaviour of Nephrops norvegicus. , 2013, Advances in marine biology.

[67]  Paolo Menesatti,et al.  A new morphometric implemented video-image analysis protocol for the study of social modulation in activity rhythms of marine organisms , 2009, Journal of Neuroscience Methods.