Multisensory Integration and Behavioral Plasticity in Sharks from Different Ecological Niches

The underwater sensory world and the sensory systems of aquatic animals have become better understood in recent decades, but typically have been studied one sense at a time. A comprehensive analysis of multisensory interactions during complex behavioral tasks has remained a subject of discussion without experimental evidence. We set out to generate a general model of multisensory information extraction by aquatic animals. For our model we chose to analyze the hierarchical, integrative, and sometimes alternate use of various sensory systems during the feeding sequence in three species of sharks that differ in sensory anatomy and behavioral ecology. By blocking senses in different combinations, we show that when some of their normal sensory cues were unavailable, sharks were often still capable of successfully detecting, tracking and capturing prey by switching to alternate sensory modalities. While there were significant species differences, odor was generally the first signal detected, leading to upstream swimming and wake tracking. Closer to the prey, as more sensory cues became available, the preferred sensory modalities varied among species, with vision, hydrodynamic imaging, electroreception, and touch being important for orienting to, striking at, and capturing the prey. Experimental deprivation of senses showed how sharks exploit the many signals that comprise their sensory world, each sense coming into play as they provide more accurate information during the behavioral sequence of hunting. The results may be applicable to aquatic hunting in general and, with appropriate modification, to other types of animal behavior.

[1]  Jelle Atema,et al.  Sharks need the lateral line to locate odor sources: rheotaxis and eddy chemotaxis , 2007, Journal of Experimental Biology.

[2]  S. Kajiura,et al.  Behavioral responses of batoid elasmobranchs to prey-simulating electric fields are correlated to peripheral sensory morphology and ecology. , 2014, Zoology.

[3]  Sheryl Coombs,et al.  The Mechanosensory Lateral Line: Neurobiology and Evolution , 2011 .

[4]  A. Kroese,et al.  Effects of ototoxic antibiotics on sensory hair cell functioning , 1982, Hearing Research.

[5]  S. Kajiura Electroreception in neonatal bonnethead sharks, Sphyrna tiburo , 2003 .

[6]  E. Kalko,et al.  Sequential assessment of prey through the use of multiple sensory cues by an eavesdropping bat , 2012, Naturwissenschaften.

[7]  J. Atema,et al.  Flow Sensing in Sharks: Lateral Line Contributions to Navigation and Prey Capture , 2014 .

[8]  T. Hothorn,et al.  Simultaneous Inference in General Parametric Models , 2008, Biometrical journal. Biometrische Zeitschrift.

[9]  A. Kalmijn,et al.  Electric and magnetic field detection in elasmobranch fishes. , 1982, Science.

[10]  Timothy Fitzgerald,et al.  Response of juvenile scalloped hammerhead sharks to electric stimuli. , 2009, Zoology.

[11]  Lee A. Fuiman,et al.  Function of the Free Neuromasts of Marine Teleost Larvae , 1989 .

[12]  Massimo Vergassola,et al.  ‘Infotaxis’ as a strategy for searching without gradients , 2007, Nature.

[13]  Timothy E Higham,et al.  Multidimensional analysis of suction feeding performance in fishes: fluid speed, acceleration, strike accuracy and the ingested volume of water , 2006, Journal of Experimental Biology.

[14]  T. Higham,et al.  Sucking while swimming: evaluating the effects of ram speed on suction generation in bluegill sunfish Lepomis macrochirus using digital particle image velocimetry , 2005, Journal of Experimental Biology.

[15]  R. Hueter,et al.  Diet, feeding habits, and diel feeding chronology of the bonnethead shark, Sphyrna tiburo, in southwest Florida , 1996 .

[16]  E. Hobson,et al.  Feeding Behavior in Three Species of Sharks , 1963 .

[17]  A. Kalmijn,et al.  The electric sense of sharks and rays. , 1971, The Journal of experimental biology.

[18]  L. Palmer,et al.  Effect of the anesthetic tricaine (MS-222) on nerve activity in the anterior lateral line of the oyster toadfish, Opsanus tau. , 2004, Journal of neurophysiology.

[19]  A. Thesis FEEDING HABITS OF BLACKTIP SHARKS, CARCHARHINUS LIMBATUS, AND ATLANTIC SHARPNOSE SHARKS, RHIZOPRIONODON TERRAENOVAE, IN LOUISIANA COASTAL WATERS , 2002 .

[20]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[21]  Gary C. Packard,et al.  The use of percentages and size-specific indices to normalize physiological data for variation in body size: wasted time, wasted effort? , 1999 .

[22]  T. Takagi,et al.  Schooling behaviour of juvenile Pacific bluefin tuna Thunnus orientalis depends on their vision development. , 2011, Journal of fish biology.

[23]  Shane P. Windsor,et al.  The flow fields involved in hydrodynamic imaging by blind Mexican cave fish (Astyanax fasciatus). Part II: gliding parallel to a wall , 2010, Journal of Experimental Biology.

[24]  André W. Visser,et al.  Predation vulnerability of planktonic copepods: consequences of predator foraging strategies and prey sensory abilities , 1998 .

[25]  R. Sheldon The sense of smell in Selachians , 1911 .

[26]  Eric Parmentier,et al.  Fish lateral system is required for accurate control of shoaling behaviour , 2010, Animal Behaviour.

[27]  G. Arnold,et al.  RHEOTROPISM IN FISHES , 1974, Biological reviews of the Cambridge Philosophical Society.

[28]  J. Castro The Biology of the Nurse Shark, Ginglymostoma cirratum, Off the Florida East Coast and the Bahama Islands , 2000, Environmental Biology of Fishes.

[29]  S. J. Arnold,et al.  Morphology, Performance and Fitness , 1983 .

[30]  Perry W. Gilbert,et al.  Sharks and survival , 1966 .

[31]  Jelle Atema,et al.  The Function of Bilateral Odor Arrival Time Differences in Olfactory Orientation of Sharks , 2010, Current Biology.

[32]  P. Motta,et al.  Largemouth bass (Micropterus salmoides) switch feeding modalities in response to sensory deprivation. , 2012, Zoology.

[33]  Ad. J. Kalmijn,et al.  The Detection of Electric Fields from Inanimate and Animate Sources Other Than Electric Organs , 1974 .

[34]  J. Lagardère,et al.  No efficiency of the lateral system on nocturnal feeding in the European sea bass (Dicentrarchus labrax L.) , 2006 .

[35]  J. Lagardère,et al.  Impact of acute cadmium exposure on the trunk lateral line neuromasts and consequences on the "C-start" response behaviour of the sea bass (Dicentrarchus labrax L.; Teleostei, Moronidae). , 2006, Aquatic toxicology.

[36]  The Sense-organs and Perceptions of Fishes ; with Remarks on the Supply of Bait , 2005 .

[37]  Jelle Atema,et al.  Sensory Biology of Aquatic Animals , 1988, Springer New York.

[38]  Shaun P. Collin,et al.  Sensory Processing in Aquatic Environments , 2011, Springer New York.

[39]  K. Holland,et al.  Electroreception in juvenile scalloped hammerhead and sandbar sharks. , 2002, The Journal of experimental biology.

[40]  R. Hueter Adaptations for spatial vision in sharks , 1990 .

[41]  D. Nelson,et al.  Sharks: Attraction by Low-Frequency Sounds , 1963, Science.

[42]  M. McFall-Ngai Crypsis in the Pelagic Environment , 1990 .

[43]  I. Tibbetts,et al.  Electric Field Detection in Sawfish and Shovelnose Rays , 2012, PloS one.

[44]  K. Gravitte A Foray into the Worlds of Animals and Humans, with A Theory of Meaning , 2012 .

[45]  C. Prange,et al.  Movements of cephalic components during feeding in some requiem sharks (Carcharhiniformes: Carcharhinidae) , 1987 .

[46]  C. Brönmark,et al.  Chemical Ecology in Aquatic Systems , 2012 .

[47]  David Doubilet Light in the Sea , 2022, World Literature Today.

[48]  C. F. Baker,et al.  The sensory basis of rheotaxis in the blind Mexican cave fish, Astyanax fasciatus , 1999, Journal of Comparative Physiology A.

[49]  S. Kajiura,et al.  Electroreception in the euryhaline stingray, Dasyatis sabina , 2009, Journal of Experimental Biology.

[50]  P. Motta,et al.  Durophagy in sharks: feeding mechanics of the hammerhead Sphyrna tiburo. , 2000, The Journal of experimental biology.

[51]  R F Mathewson,et al.  Klinotaxis and rheotaxis in orientation of sharks toward chemical stimuli. , 1972, Comparative biochemistry and physiology. A, Comparative physiology.

[52]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[53]  M. Sanders Handbook of Sensory Physiology , 1975 .

[54]  R. Mathewson,et al.  CHEMOSENSORY ORIENTATION IN SHARKS * , 1971, Annals of the New York Academy of Sciences.

[55]  L. Ferry‐Graham,et al.  Effects of prey size and mobility on prey-capture kinematics in leopard sharks triakis semifasciata , 1998, The Journal of experimental biology.

[56]  Edward S. Hodgson,et al.  Sensory biology of sharks, skates, and rays , 1978 .

[57]  K. Kardong,et al.  Sensory Deprivation Effects on the Predatory Behavior of the Rattlesnake, Crotalus viridis oreganus , 1996 .

[58]  T. Tricas,et al.  On the attraction of larval fishes to reef sounds , 2007 .

[59]  J. Gardiner Multisensory Integration in Shark Feeding Behavior , 2012 .

[60]  S. Gruber,et al.  The behavior of the bonnethead shark, Sphyrna tiburo , 1974 .

[61]  E. P. Lyon ON RHEOTROPISM. I. — RHEOTROPISM IN FISHES , 1904 .

[62]  P. Ridd,et al.  Range of electrosensory detection of prey by Carcharhinus melanopterus and Himantura granulata , 2001 .

[63]  Christoph Brücker,et al.  Measuring Flow Velocity and Flow Direction by Spatial and Temporal Analysis of Flow Fluctuations , 2008, The Journal of Neuroscience.

[64]  S. Coombs,et al.  Nearfield detection of dipole sources by the goldfish (Carassius auratus) and the mottled sculpin (Cottus bairdi). , 1994, The Journal of experimental biology.

[65]  G. Lauder,et al.  Quantification of flow during suction feeding in bluegill sunfish. , 2003, Zoology.

[66]  F. James Rohlf,et al.  Biometry: The Principles and Practice of Statistics in Biological Research , 1969 .

[67]  R. Raguso,et al.  Sensory flexibility in hawkmoth foraging behavior: lessons from Manduca sexta and other species. , 2005, Chemical senses.

[68]  Adam P. Summers,et al.  Functional morphology of the feeding apparatus, feeding constraints, and suction performance in the nurse shark Ginglymostoma cirratum , 2008, Journal of morphology.

[69]  D. Nelson,et al.  Prey Capture by the Pacific Angel Shark, Squatina californica: Visually Mediated Strikes and Ambush-Site Characteristics , 1999 .

[70]  M. Peach The behavioural role of pit organs in the epaulette shark , 2003 .

[71]  Prof. Dr. Eberhard Curio The Ethology of Predation , 1976, Zoophysiology and Ecology.

[72]  N. Scholz,et al.  Olfactory toxicity in fishes. , 2010, Aquatic toxicology.

[73]  T. Stanford,et al.  Multisensory integration: current issues from the perspective of the single neuron , 2008, Nature Reviews Neuroscience.

[74]  E. Hassan Hydrodynamic Imaging of the Surroundings by the Lateral Line of the Blind Cave Fish Anoptichthys jordani , 1989 .

[75]  S. Kajiura Head Morphology and Electrosensory Pore Distribution of Carcharhinid and Sphyrnid Sharks , 2001, Environmental Biology of Fishes.

[76]  N. Vickers Mechanisms of animal navigation in odor plumes. , 2000, The Biological bulletin.

[77]  Prey capture in frogs: alternative strategies, biomechanical trade-offs, and hierarchical decision making. , 2011, Journal of experimental zoology. Part A, Ecological genetics and physiology.

[78]  Ronald L. Woodfin,et al.  Trace chemical sensing of explosives , 2007 .

[79]  J. Janssen,et al.  Use of the lateral line and tactile senses in feeding in four antarctic nototheniid fishes , 1996, Environmental Biology of Fishes.

[80]  G. Lauder,et al.  Aquatic prey capture in ray‐finned fishes: A century of progress and new directions , 2001, Journal of morphology.

[81]  A. Tester,et al.  The Role of Olfaction in Shark Predation , 1963 .

[82]  J. Atema Aquatic odour dispersal fields , 2012 .

[83]  M. Gordon,et al.  Functional consequences of structural differences in stingray sensory systems. Part II: electrosensory system , 2009, Journal of Experimental Biology.

[84]  R. Holzman,et al.  How to surprise a copepod: Strike kinematics reduce hydrodynamic disturbance and increase stealth of suction‐feeding fish , 2009 .

[85]  G. Ruxton Non-visual crypsis: a review of the empirical evidence for camouflage to senses other than vision , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[86]  Shane P. Windsor,et al.  The flow fields involved in hydrodynamic imaging by blind Mexican cave fish (Astyanax fasciatus). Part I: open water and heading towards a wall , 2010, Journal of Experimental Biology.

[87]  Clemens Lakner,et al.  Elasmobranch Phylogeny: A Mitochondrial Estimate Based on 595 Species , 2012 .

[88]  L. Palmer,et al.  Sensitivity of the anterior lateral line to natural stimuli in the oyster toadfish, Opsanus tau (Linnaeus) , 2005, Journal of Experimental Biology.

[89]  J. Gray,et al.  Mechanical Factors in the Excitation of the Lateral Lines of Fishes , 1988 .

[90]  K. Ikeda,et al.  Effects of streptomycin, kanamycin, quinine, and other drugs on the microphonic potentials of goldfish sacculus. , 1971, The Japanese journal of physiology.

[91]  A. Kalmijn,et al.  Bioelectric Fields in Sea Water and the Function of the Ampullae of Lorenzini in Elasmobranch Fishes , 1972 .

[92]  Ad. J. Kalmijn,et al.  Hydrodynamic and Acoustic Field Detection , 1988 .

[93]  T. Tricas,et al.  Enhanced visual fields in hammerhead sharks , 2009, Journal of Experimental Biology.

[94]  B. Siemers,et al.  The sensory basis of prey detection in captive-born grey mouse lemurs, Microcebus murinus , 2008, Animal Behaviour.

[95]  G. Lauder,et al.  Hydrodynamics of prey capture in sharks: effects of substrate , 2007, Journal of The Royal Society Interface.

[96]  Jelle Atema,et al.  The importance of the lateral line in nocturnal predation of piscivorous catfish , 2004, Journal of Experimental Biology.

[97]  J. Castro Biology of the blacktip shark, Carcharhinus limbatus, off the Southeastern United States , 1996 .

[98]  John C. Montgomery,et al.  The sensory basis of olfactory search behavior in banded kokopu (Galaxias fasciatus) , 2002, Journal of Comparative Physiology A.

[99]  S. Coombs,et al.  Feeding and orientation of mottled sculpin, Cottus bairdi, to water jets , 1990, Environmental Biology of Fishes.

[100]  S. Coombs,et al.  The orienting response of Lake Michigan mottled sculpin is mediated by canal neuromasts. , 2001, The Journal of experimental biology.

[101]  Arthur A. Myrberg,et al.  The Acoustical Biology of Elasmobranchs , 2001, Environmental Biology of Fishes.

[102]  Frank W. Grasso,et al.  Integration of Flow and Chemical Sensing for Guidance of Autonomous Marine Robots in Turbulent Flows , 2002 .

[103]  W. Bateson,et al.  The Sense-organs and Perceptions of Fishes; with Remarks on the Supply of Bait , 1890, Journal of the Marine Biological Association of the United Kingdom.

[104]  Donald R. Webster Structure of Turbulent Chemical Plumes , 2006 .

[105]  E. Hassan,et al.  Studies on the effects of Ca2++ and Co++ on the swimming behavior of the blind Mexican cave fish , 1992, Journal of Comparative Physiology A.

[106]  F. Ladich,et al.  Effects of ship noise on the detectability of communication signals in the Lusitanian toadfish , 2007, Journal of Experimental Biology.

[107]  S Kaus,et al.  The Effect of Aminoglycoside Antibiotics on the Lateral Line Organ of Aplocheilus lineatus (Cyprinodontidae). , 1987, Acta oto-laryngologica.