Environment-dependent prey capture in the Atlantic mudskipper (Periophthalmus barbarus)

ABSTRACT Few vertebrates capture prey in both the aquatic and the terrestrial environment due to the conflicting biophysical demands of feeding in water versus air. The Atlantic mudskipper (Periophthalmus barbarus) is known to be proficient at feeding in the terrestrial environment and feeds predominately in this environment. Given the considerable forward flow of water observed during the mouth-opening phase to assist with feeding on land, the mudskipper must alter the function of its feeding system to feed successfully in water. Here, we quantify the aquatic prey-capture kinematics of the mudskipper and compare this with the previously described pattern of terrestrial feeding. Prior to feeding in the aquatic environment, the gill slits open, allowing water to be expelled through the gill slits. The opposite happens in terrestrial feeding during which the gill slits remain closed at this point. In water, the expansive movements of the head are larger, amounting to a larger volume increase and are initiated slightly later than in the terrestrial environment. This implies the generation of strong suction flows when feeding in water. Consequently, the kinematic patterns of the hydrodynamic tongue during terrestrial feeding and aquatic suction feeding are similar, except for the amplitude of the volume increase and the active closing of the gill slits early during the terrestrial feeding strike. The mudskipper thus exhibits the capacity to change the kinematics of its feeding apparatus to enable successful prey capture in two disparate environments. Summary: A comparison of the kinematics of aquatic and terrestrial feeding in the mudskipper shows how the ancestral kinematic pattern of aquatic feeding is modified to enable the terrestrial capture of prey.

[1]  P. Aerts,et al.  A fish that uses its hydrodynamic tongue to feed on land , 2015, Proceedings of the Royal Society B: Biological Sciences.

[2]  P. Aerts,et al.  Functional anatomy and kinematics of the oral jaw system during terrestrial feeding in Periophthalmus barbarus , 2014, Journal of morphology.

[3]  P. Aerts,et al.  Masters of change: seasonal plasticity in the prey-capture behavior of the Alpine newt Ichthyosaura alpestris (Salamandridae) , 2013, Journal of Experimental Biology.

[4]  S. V. Wassenbergh,et al.  Kinematics of terrestrial capture of prey by the eel-catfish Channallabes apus. , 2013 .

[5]  P. Aerts,et al.  Biomechanical Studies of Food and Diet Selection , 2012 .

[6]  C. T. Stayton Terrestrial feeding in aquatic turtles: environment-dependent feeding behavior modulation and the evolution of terrestrial feeding in Emydidae , 2011, Journal of Experimental Biology.

[7]  J. L. Leeuwen,et al.  Optimum sucking techniques for predatory fish , 2010 .

[8]  M. Muller,et al.  Hydrodynamics of suction feeding in fish , 2010 .

[9]  P. Aerts,et al.  Hydrodynamic constraints on prey-capture performance in forward-striking snakes , 2010, Journal of The Royal Society Interface.

[10]  G. Lauder,et al.  Terrestrial feeding in the Mudskipper Periophthalmus (Pisces: Teleostei): A cineradiographic analysis , 2009 .

[11]  P. Aerts,et al.  Intrinsic Mechanics and Control of Fast Cranio-Cervical Movements in Aquatic Feeding Turtles1 , 2001 .

[12]  E. Brainerd,et al.  Kinematics of aquatic and terrestrial prey capture in Terrapene carolina, with implications for the evolution of feeding in cryptodire turtles. , 1998, The Journal of experimental zoology.

[13]  W. Bemis,et al.  Functional morphology of tongue projection in Taricha torosa (Urodela: Salamandridae) , 1990 .

[14]  M. Drost,et al.  A simple method for measuring the changing volume of small biological objects, illustrated by studies of suction feeding by fish larvae and of shrinkage due to histological fixation , 1986 .

[15]  H. Shaffer,et al.  Functional morphology of the feeding mechanism in aquatic ambystomatid salamanders , 1985, Journal of morphology.

[16]  H. Shaffer,et al.  PATTERNS OF VARIATION IN AQUATIC AMBYSTOMATID SALAMANDERS: KINEMATICS OF THE FEEDING MECHANISM , 1985, Evolution; international journal of organic evolution.

[17]  M S Gordon,et al.  Aspects of the physiology of terrestrial life in amphibious fishes. II. The Chilean clingfish, Sicyases sanguineus. , 1969, The Journal of experimental biology.

[18]  Robert C. Stebbins,et al.  Observations on the Natural History of the Mud-skipper, Periophthalmus sobrinus , 1961 .

[19]  S. Van Wassenbergh Kinematics of terrestrial capture of prey by the eel-catfish Channallabes apus. , 2013, Integrative and comparative biology.

[20]  J. L. Leeuwen,et al.  Muscle activation and strain patterns of the m. hyohyoideus of carp (Cyprinus carpio L.) during opercular movements , 2003 .

[21]  U. Morphology,et al.  Aquatic Feeding in Salamanders , 2000 .

[22]  Kurt Schwenk,et al.  Feeding : form, function, and evolution in tetrapod vertebrates , 2000 .

[23]  K. Schwenk CHAPTER 2 – An Introduction to Tetrapod Feeding , 2000 .

[24]  D. Wake,et al.  CHAPTER 3 – Aquatic Feeding in Salamanders , 2000 .