New insights from serranid fishes on the role of trade-offs in suction-feeding diversification

SUMMARY Suction feeding is central to prey capture in the vast majority of ray-finned fishes and has been well studied from a detailed, mechanistic perspective. Several major trade-offs are thought to have shaped the diversification of suction-feeding morphology and behavior, and have become well established in the literature. We revisited several of these expectations in a study of prey capture morphology and kinematics in 30 species of serranid fishes, a large, ecologically variable group that exhibits diverse combinations of suction and forward locomotion. We find that: (1) diversity among species in the morphological potential to generate suction changes drastically across the range of attack speeds that species use, with all species that use high-speed attacks having low capacity to generate suction, whereas slow-speed attackers exhibit the full range of suction abilities (this pattern indicates a more complex ‘ram–suction continuum’ than previously recognized); (2) there is no trade-off between the mechanical advantage of the lower jaw opening lever and the speed of jaw depression, revealing that this simple interpretation of lever mechanics fails to predict kinematic diversity; (3) high-speed attackers show increased cranial excursions, potentially to compensate for a decrease in accuracy; (4) the amount of jaw protrusion is positively related to attack speed, but not suction capacity; and (5) a principal component analysis revealed three significant multivariate axes of kinematic variation among species. Two of the three axes were correlated with the morphological potential to generate suction, indicating important but complex relationships between kinematics and suction potential. These results are consistent with other recent studies that show that trade-offs derived from simple biomechanical models may be less of a constraint on the evolutionary diversification of fish feeding systems than previously thought.

[1]  D. Bellwood,et al.  A Functional morphospace for the skull of labrid fishes: patterns of diversity in a complex biomechanical system , 2004 .

[2]  R. Holzman,et al.  Scaling of suction-induced flows in bluegill: morphological and kinematic predictors for the ontogeny of feeding performance , 2008, Journal of Experimental Biology.

[3]  A. M. Carroll,et al.  Morphology predicts suction feeding performance in centrarchid fishes , 2004, Journal of Experimental Biology.

[4]  G. Johnson,et al.  PHYLOGENY OF THE EPINEPHELINAE (TELEOSTEI: SERRANIDAE) , 1993 .

[5]  Peter C Wainwright,et al.  Feeding mechanism of Epibulus insidiator (Labridae; Teleostei): Evolution of a novel functional system , 1989, Journal of morphology.

[6]  B. Flammang,et al.  Prey capture kinematics and four-bar linkages in the bay pipefish, Syngnathus leptorhynchus. , 2009, Zoology.

[7]  L. Ferry‐Graham,et al.  Premaxillary movements in cyprinodontiform fishes: an unusual protrusion mechanism facilitates "picking" prey capture. , 2008, Zoology.

[8]  Tyson L Hedrick,et al.  Software techniques for two- and three-dimensional kinematic measurements of biological and biomimetic systems , 2008, Bioinspiration & biomimetics.

[9]  J. L. Leeuwen A quantitative study of flow in prey capture by Rainbow trout, Salmo gairdneri with general consideration of the actinopterygian feeding mechanism , 2010 .

[10]  Donald A. Jackson STOPPING RULES IN PRINCIPAL COMPONENTS ANALYSIS: A COMPARISON OF HEURISTICAL AND STATISTICAL APPROACHES' , 1993 .

[11]  C. D. Hulsey,et al.  Feeding with speed: prey capture evolution in cichilds , 2007, Journal of evolutionary biology.

[12]  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.

[13]  R. Holzman,et al.  Jaw protrusion enhances forces exerted on prey by suction feeding fishes , 2008, Journal of The Royal Society Interface.

[14]  D. Nemeth,et al.  Modulation of attack behavior and its effect on feeding performance in a trophic generalist fish, , 1997, The Journal of experimental biology.

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

[16]  P. Sale Coral reef fishes : dynamics and diversity in a complex ecosystem , 2002 .

[17]  C. D. Hulsey,et al.  Cichlid jaw mechanics: linking morphology to feeding specialization , 2005 .

[18]  T. Higham,et al.  Spatial and temporal patterns of water flow generated by suction-feeding bluegill sunfish Lepomis macrochirus resolved by Particle Image Velocimetry , 2005, Journal of Experimental Biology.

[19]  P. Motta,et al.  A comparison of strike and prey capture kinematics of three species of piscivorous fishes: Florida gar (Lepisosteus platyrhincus), redfin needlefish (Strongylura notata), and great barracuda (Sphyraena barracuda) , 2004 .

[20]  W. Taylor,et al.  Revised procedures for staining and clearing small fishes and other vertebrates for bone and cartilage study , 1985 .

[21]  Gibb Do flatfish feed like other fishes? A comparative study of percomorph prey-capture kinematics. , 1997, The Journal of experimental biology.

[22]  P. Hastings,et al.  A molecular phylogeny of the groupers of the subfamily Epinephelinae (Serranidae) with a revised classification of the Epinephelini , 2007, Ichthyological Research.

[23]  T. Garland,et al.  Procedures for the Analysis of Comparative Data Using Phylogenetically Independent Contrasts , 1992 .

[24]  P. Wainwright,et al.  Effects of ram speed on prey capture kinematics of juvenile Indo-Pacific tarpon, Megalops cyprinoides. , 2010, Zoology.

[25]  T. Higham Feeding, fins and braking maneuvers: locomotion during prey capture in centrarchid fishes , 2007, Journal of Experimental Biology.

[26]  P C Wainwright,et al.  Evaluating the use of ram and suction during prey capture by cichlid fishes. , 2001, The Journal of experimental biology.

[27]  A. M. Carroll Muscle activation and strain during suction feeding in the largemouth bass Micropterus salmoides , 2004, Journal of Experimental Biology.

[28]  E. Brainerd,et al.  CONVERGENCE IN THE FEEDING MECHANICS OF ECOMORPHOLOGICALLY SIMILAR SPECIES IN THE CENTRARCHIDAE AND CICHLIDAE , 1993 .

[29]  P. Aerts,et al.  Modulation and variability of prey capture kinematics in clariid catfishes. , 2006, Journal of experimental zoology. Part A, Comparative experimental biology.

[30]  M. Westneat,et al.  Form and function of damselfish skulls: rapid and repeated evolution into a limited number of trophic niches , 2009, BMC Evolutionary Biology.

[31]  K. Liem Acquisition of Energy by Teleosts: Adaptive Mechanisms and Evolutionary Patterns , 1980 .

[32]  M. Craig,et al.  Casting the Percomorph Net Widely: The Importance of Broad Taxonomic Sampling in the Search for the Placement of Serranid and Percid Fishes , 2007, Copeia.

[33]  P. Wainwright,et al.  Predicting patterns of prey use from morphology of fishes , 1995, Environmental Biology of Fishes.

[34]  R. Holzman,et al.  Integrating the determinants of suction feeding performance in centrarchid fishes , 2008, Journal of Experimental Biology.

[35]  E. Bermingham,et al.  Genetic mosaic in a marine species flock , 2003, Molecular ecology.

[36]  D. Bellwood,et al.  Modulation of prey capture kinematics in the cheeklined wrasse Oxycheilinus digrammus (Teleostei: Labridae). , 2001, The Journal of experimental zoology.

[37]  C. Marshall,et al.  Feeding biomechanics of juvenile red snapper (Lutjanus campechanus) from the northwestern Gulf of Mexico , 2008, Journal of Experimental Biology.

[38]  DISCORDANCE BETWEEN MORPHOLOGICAL AND MECHANICAL DIVERSITY IN THE FEEDING MECHANISM OF CENTRARCHID FISHES , 2006 .

[39]  S. Day,et al.  The forces exerted by aquatic suction feeders on their prey , 2007, Journal of The Royal Society Interface.

[40]  P. Aerts,et al.  Kinematics and functional morphology of aquatic feeding in Australian snake‐necked turtles (Pleurodira; Chelodina) , 1997, Journal of morphology.

[41]  Peter C Wainwright,et al.  Muscle function and power output during suction feeding in largemouth bass, Micropterus salmoides. , 2006, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[42]  O Shoval,et al.  Evolutionary Trade-Offs, Pareto Optimality, and the Geometry of Phenotype Space , 2012, Science.

[43]  P. Motta Mechanics and Functions of Jaw Protrusion in Teleost Fishes: A Review , 1984 .

[44]  G. Lauder The Suction Feeding Mechanism in Sunfishes (Lepomis): An Experimental Analysis , 1980 .

[45]  Peter Wainwright,et al.  Suction feeding mechanics, performance, and diversity in fishes. , 2007, Integrative and comparative biology.

[46]  M. Westneat,et al.  Transmission of force and velocity in the feeding mechanisms of labrid fishes (Teleostei, Perciformes) , 1994, Zoomorphology.

[47]  A. M. Carroll,et al.  Scaling of In Vivo Muscle Velocity during Feeding in the Largemouth Bass, Micropterus salmoides (Centrarchidae) , 2011, Physiological and Biochemical Zoology.

[48]  M. Westneat,et al.  Evolution of Levers and Linkages in the Feeding Mechanisms of Fishes1 , 2004, Integrative and comparative biology.

[49]  R. Holzman,et al.  Co-evolution of the premaxilla and jaw protrusion in cichlid fishes (Heroine: Cichlidae) , 2010 .

[50]  D. Pondella,et al.  On the status of the Serranid fish genus Epinephelus: evidence for paraphyly based upon 16S rDNA sequence. , 2001, Molecular phylogenetics and evolution.

[51]  R. Holzman,et al.  Biomechanical trade-offs bias rates of evolution in the feeding apparatus of fishes , 2012, Proceedings of the Royal Society B: Biological Sciences.

[52]  S. V. Wassenbergh,et al.  Piscivorous cyprinid fish modulates suction feeding kinematics to capture elusive prey. , 2011 .

[53]  P. Wainwright,et al.  Functional morphology of extreme jaw protrusion in Neotropical cichlids , 2003, Journal of morphology.

[54]  R. Holzman,et al.  Functional Complexity Can Mitigate Performance Trade-Offs , 2011, The American Naturalist.

[55]  T. Higham,et al.  The integration of locomotion and prey capture in divergent cottid fishes: functional disparity despite morphological similarity , 2011, Journal of Experimental Biology.

[56]  G. Lauder,et al.  Prey capture by Luciocephalus pulcher: implications for models of jaw protrusion in teleost fishes , 1981, Environmental Biology of Fishes.

[57]  J. E. Randall Food habits of reef fishes of the West Indies , 1967 .

[58]  D. Bellwood,et al.  Functional versatility supports coral reef biodiversity , 2006, Proceedings of the Royal Society B: Biological Sciences.

[59]  P. Aerts,et al.  No trade-off between biting and suction feeding performance in clariid catfishes , 2007, Journal of Experimental Biology.

[60]  J. Felsenstein Phylogenies and the Comparative Method , 1985, The American Naturalist.

[61]  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.

[62]  There is no trade-off between speed and force in a dynamic lever system , 2011, Biology Letters.

[63]  David R. Bellwood,et al.  Ecomorphology of feeding in coral reef fishes , 2002 .

[64]  Lara A Ferry,et al.  Prey capture behavior of native vs. nonnative fishes: a case study from the Colorado River drainage basin (USA). , 2012, Journal of experimental zoology. Part A, Ecological genetics and physiology.

[65]  P. Aerts,et al.  Aquatic suction feeding dynamics: insights from computational modelling , 2009, Journal of The Royal Society Interface.

[66]  D. Collar,et al.  DISCORDANCE BETWEEN MORPHOLOGICAL AND MECHANICAL DIVERSITY IN THE FEEDING MECHANISM OF CENTRARCHID FISHES , 2006, Evolution; international journal of organic evolution.

[67]  P. Motta,et al.  A comparison of prey capture kinematics in hatchery and wild Micropterus salmoides floridanus: effects of ontogeny and experience , 2005 .

[68]  R. Holzman,et al.  An integrative modeling approach to elucidate suction-feeding performance , 2012, Journal of Experimental Biology.

[69]  L. Ferry‐Graham,et al.  Cranial movements during suction feeding in teleost fishes: Are they modified to enhance suction production? , 2005, Zoology.

[70]  A. Biewener,et al.  There is always a trade-off between speed and force in a lever system: comment on McHenry (2010) , 2011, Biology Letters.

[71]  A force–speed trade-off is not absolute , 2011, Biology Letters.