Anatomy and physiology in Centrarchid fishes demonstrates a functional correlation of feeding behavior with biomechanics

Madison Byrne, Jeri Rosenbloom, Paul Gignac, Nicholas J GidmarkKnox College Department of Biology, Galesburg, IL

Oklahoma State University, Stillwater, OK

Ram Suction

Abstract

Musculoskeletal anatomy varies widely across vertebrates, and the main driver of that variation is functional performance at the organismal level. One of the most impactful selective pressures on an organism is food acquisition, therefore musculoskeletal anatomy should vary across prey capture method. Nearly all aquatic animals get their food by sucking water into their mouth. Suction feeding is a highly synchronized process necessitating kinetic skull bones and recruiting muscles from the whole body that results in fluid flow into the mouth, transporting prey towards the predator. However, suction isn’t the only feeding behavior in fishes; some also approach their prey to attack via engulfing it, a behavior termed “ram feeding”. In fishes, feeding behavior spans a spectrum from pure ram-feeding to pure suction-feeding. Ram-feeding has different optimality criteria and uses completely different muscles, so we expect that anatomy and performance will vary in fishes across the ram-suction index. The family Centrarchidae is a great model system for examining the form-function relationship in fishes, because this small group spans the entirety of the ram-suction index. Herein, we examine two aspects of functional anatomy in Centrarchids: in situ muscle contractile performance (Chapter 1) and skeletal anatomy (Chapter 2). To examine variation in muscle performance, we supra-maximally stimulated the jaw adductor of individuals from five species of Centrarchid at a variety of gape angels and jaw-closing velocities. To examine morphological differences in the skeleton, we micro-CT scanned the entire family of Centrarchidae and measured twelve aspects of skull shape. Both jaw adductor performance and skull shape varied with feeding behavior. Ram feeding species, as well as species that crushed prey, had adductors that were faster and stronger than their suction-feeding counterparts. There was a clear correlation of some aspects of skull shape with the ram-suction index. These aspects clearly highlighted biomechanically advantageous morphology for suction feeding (premaxilla length, epaxial muscle size) and ram feeding (high jaw-closing muscle attachment angle). Not all of the variation in skull shape could be accounted for by feeding ecology -- mouth size varied independently of the ram-suction index. The morphology and performance of the skull is dominated by feeding behavior along the ram-suction index, but is influenced by selective pressures from other ecological behaviors.

Physiological and Biomechanical Limits

Centrarchidae as a model system

Experimental Physiology Approach

Anatomical Correlation with Feeding Behavior

Discussion and Conclusions:

● Adductor muscle performance varied by feeding ecology

● Skeletal morphology varied markedly across the ram-suction index

● Not all of the variation within the skeleton can be attributed to this continuum, as mouth size varied independently of ram or suction

● Although a fish’s skull is under many selective pressures, the skeleton and adjacent muscles adapt to specialize in specific feeding behaviors

Anatomical Correlation with Feeding Behavior

Acknowledgments:

We thank the Richter Memorial Grant and the ASSET program for funding this research, the Illinois Natural History Survey for access to specimens, and the Ellen Browning Scripps Foundation for support of the Knox College Makerspace.

Performospace

#1

length-tension Example Trial

Force-Velocity Example Trial

Figure 6. Raw traces of jaw position (blue) and force (red) from the lever motor over time. Region of interest (green) was extracted from raw trace based on custom-written R code algorhythms.

Figure 7. Multiple trials for a given individual are conducted at multiple lengths (left) or force thresholds (right), resulting in variation in maximum force (left) and contractile velocities (right), due to length-tension and force-velocity constraints on skeletal muscle.

Figure 8. All trials for a single individual are aggregated to plot length-tension or force-velocity relationships for each individual. All colors in this figure match trials from Fig. 7.

Figure 14. Schematic of axises of variation within the PCA. The ram-suction index runs diagonally from the bottom left and upper right. On a diagonal from the top left to the bottom right, the mouth of the fish gets smaller to larger, independent of the ram-suction index. Examples of skull shape from each quadrant are shown, with the blackbanded sunfish, green sunfish, shoal bass, and Sacramento perch as representatives.

Figure 10. Examples of metrics used for analysis. Metric 1: Gape at peak force. Metric 2: Gape range at 90% of peak force. Metric 3: Time to peak tension. Metric 4: Time to relaxation. Metric 5: Absolute force production. Metric 6: Gape range. Metric 7: Relative force at 3mm/second. Metric 8: Velocity at 65% peak force. Metric 9: a-coefficient of polynomial regression. Metric 10: b-coefficient of polynomial regression.

Figure 11. Principal component analysis of principal components one and two that accounts for 71.7% of variation in our length-tension experiments. Relative gape at peak force (1), percent gape at 90% peak force (2), time to peak tension (3), and gape range (6) drive an individual to the right of PC 1, while absolute force production (5) drives placement to the upper right quadrant, and time to relaxation (4) pushes an individual to the upper left quadrant.

Figure 13. Principal components one and two account for 73.34% of variation across anatomical metrics. Data points are color coded according to genus: Lepomis in blue, Micropterus in red, and other genera in green. The black arrows show how each metric influences the position of the species. Muscle attachment angle drives position down to the left, while ascending premaxilla length, opening in-lever length, expaxial height and width, and head height and width drive species towards the upper right quadrant. Lever ratio drives species up and to the left, and in-lever, out-lever, maxilla, and premaxilla length move species towards the bottom right.

Figure 12. Principal component analysis of principal components one and two that accounts for 91.5% of variation. Relative force at 3mm/sec (7) and velocity at 65% peak force (8) drive placement to the upper right quadrant, while the A-coefficient (9) pulls the data point down and slightly to the right. The B-coefficient (10) is the only metric drawing data to the left of PC1.

Figure 9. Relationships from Fig 8 can be aggregated across individuals to examine species-specific difference. Here, graphs are scaled to peak force at zero velocity (P0) and colored by species: largemouth bass (purple), green sunfish (green), redear sunfish (red), black crappie (black), and bluegill sunfish (blue).

We gathered data from twenty eight individuals of five species: largemouth bass, green sunfish, black crappie, redear sunfish, and bluegill sunfish. Each in-situ trial used a servo motor and bilateral stimulations of the jaw adductor muscles. We recorded force & length at the tip of the jaw while the head was held stable. We recorded several (8-20) stimulation trials for each individual.

We quantified ten metrics of muscle physiological performance, and then used principal component analyses to spatially compare individuals within the performospace.

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Figure 4. Large family of freshwater fishes comprised of sunfish and bass. Modified from Aday et al. (2009).

Figure 5. Largemouth bass ram-feeding v.s. Bluegill sunfish suction feeding. This family has representation from both extremes of the ram-suction index as well as everywhere in between. Modified from Wainwright Lab (2012).

Figure 1. Sarcomere structure in skeletal muscle physically limits the performance of muscle across lengths and velocities. Modified from Plotnikov et al. (2006).

Figure 2. Arrangement of muscle fibers dictates whether a muscle is fast and weak (left) or slow and strong (right). Modified from Liem et al (2001).

Figure 3. The shape and size of the skeleton will be fundamentally important to the performance of an organism, and what drives size and shape is the function of the bone.

#3#4

y(x) = intercept + a(x) + b(x²)#2 #7#8

#5

#6

Blackbanded Sunfish Green Sunfish

Sacramento PerchShoal Bass

Blackbanded Sunfish Green Sunfish

Smaller Mouth

Larger MouthRam

Suction