OEB 130: Feeding Mechanisms 3 Prof. George V. Lauder The tongue-bite mechanism, feeding, and techniques

Lecture outline 1) Review of the front jaws and the pharyngeal jaws • What are the major mechanical units? • What are the major mechanical linkages? • Which muscles power jaw movement?

2) The tongue-bite mechanism 3 jaw systems in some ; Dissection (i) front (oral) jaws, (ii) pharyngeal jaws in the labs this , and (iii) a tongue-bite in between these week! two sets in the buccal cavity 3) Shark feeding mechanics

4) Functional analysis of feeding mechanisms Techniques for studying fish function: high-speed video, pressure transducers, electromyography, flow visualization

Ray-finned fish (Actinopterygii) phylogeny: broad overview

Actinopterygii (ray-finned fishes)

Holostei Chondrichthyes Polypterus and relatives Chondrostei

Teleostei

† Cheirolepis

1. Single dorsal fin 2. Fin ray structure: lepidotrichia 3. Scale structure fish phylogeny: broad overview

Otocephala

Elopomorpha Clupeiformes Ostariophysi (tarpons and eels)

Osteoglossomorpha (“bony tongues”)

Euteleostei

1. Mobile premaxilla bone in the skull 2. Specialized tail bones Teleostei 1) Review of the front jaws and the pharyngeal jaws Monocirrhus (leaffish) suction feeding 1) Review of the front jaws and the pharyngeal jaws

neurocranium Ascending process

eye operculum Pectoral girdle

suspensorium Premaxilla

maxilla

mandible Pectoral Jaw joint fin

hyoid Note: 1) Review of the front jaws and the pharyngeal jaws 1. Protrusion of the jaws during suction feeding

2. Motion of water from in front of the head, into the mouth, and then exiting behind the head after passing over the gills (not visible here).

premaxilla

Water in front of mouth Water exits opercular openings maxilla (between hyoid operculum and pectoral girdle.

1) Review of the front jaws and the pharyngeal jaws Mechanical linkages and major elements of the fish skull

Levator operculi Levator Levator Epaxial arcus operculi muscles palatini

Water in Adductor front of arcus mouth palatini BUCCAL CAVITY

Hypaxial Geniohyoideus muscles Sternohyoideus

OPERCULAR CAVITY

Muscles Oral jaws

Hyoid Ligaments apparatus

Neurocranium Pectoral girdle

Suspensorium Branchiostegal apparatus

Opercular BUCCAL CAVITY Hyoid- apparatus mandibular Operculo- ligament mandibular OPERCULAR CAVITY ligament Water exits opercular openings (between operculum and pectoral girdle. 1) Review of the front jaws and the pharyngeal jaws 1) Review of the front jaws and the pharyngeal jaws

Pharyngobranchial 1

Neurocranium Gill arches (usually 5 pairs)

2 1 3 4

Pectoral 5 girdle Premaxilla

Lower jaw Basihyal (“tongue”) Hyoid Urohyal – part of the hyoid embedded in the sternohyoideus muscle

The pharyngeal jaw apparatus (PJA) 1) Review of the front jaws and the pharyngeal jaws

Vertebra

UPJ

LPJ LPJ

LPJ: Lower pharyngeal jaw UPJ: Upper pharyngeal jaw 1) Review of the front jaws and the pharyngeal jaws

RD muscle (locate in lab if you can) Teleost fish phylogeny: broad overview

Otocephala

Elopomorpha Clupeiformes Ostariophysi (tarpons and eels)

Osteoglossomorpha (“bony tongues”)

Euteleostei

1. Mobile premaxilla bone in the skull 2. Specialized tail bones Teleostei 2) The tongue-bite mechanism: a synapomorphy of osteoglossomorph fishes Skull of an osteoglossomorph fish

1) MJA– mandibular jaw apparatus

2) PJA– pharyngeal jaw apparatus in the “throat”

3) TBA– tongue bite apparatus 2) The tongue-bite mechanism: a synapomorphy of osteoglossomorph fishes

Neurocranium

Mandible 1) MJA– mandibular jaw apparatus 2) PJA– pharyngeal jaw apparatus Hyoid 3) TBA– tongue bite apparatus Use of the tongue-bite apparatus: dramatic effect on prey

The tongue-bite behavior involves holding the prey between the upper and lower front jaws (premaxilla/maxilla, and the mandible), and then pushing the tongue teeth up and into the prey. Results of the tongue bite action on the prey Teleost fish phylogeny: broad overview

Otocephala

Elopomorpha Clupeiformes Ostariophysi (tarpons and eels)

Osteoglossomorpha (“bony tongues”)

Euteleostei

1. Mobile premaxilla bone in the skull 2. Specialized tail bones Teleostei 2) The tongue-bite mechanism: a similar system is present in some other fishes too, like salmonid fishes (salmons and relatives) 2) The tongue-bite mechanism: a similar system is present in some other fishes too

Sanford, C. P. (2001). Kinematic analysis of a novel feeding mechanism in the brook trout Salvelinus fontinalis (Teleostei: Salmonidae): behavioral modulation of a functional novelty. J. Exp. Biol. 204, 3905-3916. 3) Shark feeding mechanics Vertebrate tree – key “fish” groups 3) Shark feeding mechanics

Classic Steven Spielberg 1975 shark movie 3) Shark feeding mechanics 3) Shark feeding mechanics 3) Shark feeding mechanics

Shark bites on cables

Sharks will also bite cables towed behind ships. 3) Shark feeding mechanics

Wroe, S. et al. (2008). Three-dimensional computer analysis of white shark jaw mechanics: how hard can a great white bite? J. Zool. Lond. 276, 336-342. 3) Shark feeding mechanics

Wroe, S. et al. (2008). Three-dimensional computer analysis of white shark jaw mechanics: how hard can a great white bite? J. Zool. Lond. 276, 336-342. 3) Shark feeding mechanics 3) Shark feeding mechanics

Basking shark filter feeding 3) Shark feeding mechanics

Angel shark suction feeding 3) Shark feeding mechanics

(Great) white shark: biting 3) Shark feeding mechanics

Schematic overview of the head and jaws and gill arches 3) Shark feeding mechanics

Generally similar overall linkage systems to that of bony fishes, but rather different skeletal parts and many fewer moving elements. 3) Shark feeding mechanics

Comparing feeding systems in and bony fishes Note the color code: sharks have no opercular series 3) Shark feeding mechanics

NOTE: the palatoquadrate (upper jaw) protrudes as the mouth closes. 3) Shark feeding mechanics

NOTE: the palatoquadrate (upper jaw) protrudes as the mouth closes. 3) Shark feeding mechanics

Some images of upper jaw protrusion in elasmobranchs.

Upper row: “relaxed” jaws

Lower row: protruded palatoquadrate upper jaw 4) Functional analysis of fish feeding mechanisms

Techniques for studying fish function: A) High-speed video – to record the pattern of head motion B) Pressure transducers – to measure the suction (negative) pressure C) Electromyography – to record which muscles are active to power feeding D) Flow visualization – to directly measure flow into the mouth 4) Functional analysis of fish feeding mechanisms A) High-speed video

Side view of prey capture in the bowfin, Amia calva A) High-speed video

View from below (ventral) A) High-speed video

Kinematic pattern during suction feeding (obtained from high-speed video) Note the front-to- back timing of head movement during suction feeding: compare motions to the red dashed line. Note sequence of movement, from anterior to posterior: jaws open first, then hyoid depresses, then opercular series expands. B) Pressure transducers: quantifying suction pressure

Tube into gill (opercular) cavity Tube into mouth (buccal) cavity

Bluegill sunfish with pressure transducer cannulae in the buccal and opercular cavities B) Pressure transducers: quantifying suction pressure

Catheter-tip pressure transducer measures pressure

Pressure transducer is threaded down the plastic cannulae shown in the previous slide

The sensor is a small wire glued to the back side of the thin rubber membrane (white arrow) Measuring suction feeding pressure experimental setup

Recording equipment

Sample pressure traces Fish with tubes Measuring suction feeding pressure sample traces

Goldfish prey

Negative pressures can be very negative: -600 cm H20, for example C) Electromyography – to record which muscles are active

Inserting needle electrodes

Needle electrodes Studying muscle function in vivo: electromyography C) Electromyography – to record which muscles are active

Studying muscle function in vivo: electromyography

I. Electromyography: an important technique for studying muscle function. When electrical activity in muscles in measured, complex patterns are often observed that belie simple textbook descriptions of muscles as “flexors” or “extensors”.

II. Technique. Electrodes (either surface or needle) and amplifiers and recording devices are used to measure extracellular potentials resulting from muscle fiber membrane depolarization. Electrodes are typically bipolar and record the potential difference between the individual wires.

Inserting the electrode directly into the muscle belly is the best way to study patterns of electrical activity, but surface electrodes are often used too. Studying muscle function in vivo

Muscle 1 Muscle 1

Muscle 2

Muscle 3 Muscle 2

Sample electromyograms at two time scales. Note the multiphasic pattern of electrical activity and spike height relative to the baseline. The two traces to the left are at a shorter time scale to show a typical burst pattern recorded from white muscle fibers. The traces to the right are at an expanded time scale to better reveal the spiking pattern. EMGs can assess the relative degree of activity (properly used) and in certain cases (often involving statistical analysis of activity patterns) can be used to assess very roughly the amount of force generated by muscles.

Electromyography: measuring muscle activity in muscles during feeding and locomotion

Electrode bundle

Sunfish with electrodes in fin muscles Electromyography: measuring muscle activity in muscles during feeding

Experimental setup Sample electromyograms during prey capture, synchronized with pressure measurements Summary diagram of electromyographic activity In head muscles during prey capture in two species.

Note that the first muscle active is the levator operculi, then the epaxial and sternohyoideus muscles. These muscles power the “expansive phase”: the time when the buccal cavity volume is expanding.

Then, the major jaw closing muscle is active: the adductor mandibulae. But note the considerable overlap in activity between the mouth opening and closing muscles. Tethering prey to measure the suction force

Holzman, R., Day, S. W. and Wainwright, P. C. (2007). Timing is everything: coordination of strike kinematics affects the force exerted by suction feeding fish on attached prey. J. Exp. Biol. 210, 3328-3336. D) Flow visualization – directly measure flow into the mouth

The technique: DPIV – Digital Particle Image Velocimetry

What you do: 1) Seed the water with lots of small reflective particles

2) Use laser light spread into a thin sheet, to illuminate the particles

3) Take high-speed videos of the particles moving as prey are captured (getting fish to feed in the laser light is a trick!)

4) Analyze the particle motions to show the flow velocity field Current research: quantifying fluid flow into the mouth during prey capture by fishes. Current research: quantifying fluid flow into the mouth during prey capture by fishes. Current research: quantifying fluid flow into the mouth during prey capture by fishes. Current research: quantifying fluid flow into the mouth during prey capture by fishes. Velocity vector field resulting from a PIV analysis showing a shark attempting to eat a small piece of fish. Note the flow converging on the mouth as a result of mouth cavity expansion and pressure reduction.

Head

Mouth opening

20 mm 1.0 m s-1

0 .01 .02 .03 .04 .05 .06 .07 .08 .09 1.0 Velocity m s-1 DPIV shows the velocity gradient in front of the mouth