Tough and Stretchy: Mechanical Properties of the Alimentary Tract in a Fish Without a Stomach

Abstract

The mechanical properties of intestinal tissues determine how a thin-walled structure exerts forces on food and absorbs the force of food as it enters and travels down the gut. These properties are critically important in durophagous and stomachless fish, which must resist the potential damage to foreign bodies (e.g., shells fragments) in their diet. We test the hypothesis that the mechanical properties of the alimentary tract will differ along its length. We predict that the proximal region of the gut should be the strongest and most extensible to handle the large influx of prey often associated with stomachless fish that lack a storage depot. We developed a custom inflation technique to measure the passive mechanical properties of the whole intestine of the stomachless shiner perch, Cymatogaster aggregata. We show that mechanical properties differ significantly along the length of the alimentary tract when inflated to structural failure, with 25-46% greater maximal stress, strain, extension ratio, and toughness at the proximal (25%) position. We also find that the alimentary tissues (excluding the heavily muscular rectum) are generally highly extensible and anisotropic, and do not differ in wall circumference or thickness along the alimentary tract. These findings contribute to our knowledge of the mechanical properties of fish intestinal tissues and guide future studies of factors influencing the evolution of fish alimentary systems.

Fig. 1

(A) Photograph of the durophagous and stomachless shiner perch, Cymatogaster aggregata. (B) Extracted and unfurled “S-shaped” alimentary tract in the zero-stress state. The anterior portion begins just distal to the pharyngeal apparatus and posterior segment ends just proximal to the cloaca; scale bar = 2 cm.

Fig. 2

Representative radial cross-section showing the general wall structure of the alimentary system of the shiner perch, Cymatogaster aggregata, which consists of four layers: (1) tunica mucosa (mucosal epithelium and vascularized connective tissue), (2) submucosa (connective tissue), (3) tunica muscularis (muscle tissue), and (4) tunica serosa (mesothelial cells and vascularized connective tissue).

Fig. 3

Schematic of the pressure device used for inflation tests; see detailed description in the methods section. The break in the illustrated plastic tubing and rope indicates length changes of the material depending on height of water container, and the tray containing the intestinal segment is shown in side and top view. Applied pressures ranged from 0 to 18,100 Pa and caused gut inflations up to 8.8 mm from an initial diameter of approximately 2 mm.

Fig. 4

Representative stress-strain curve of the alimentary tract at three relative positions (25%–solid line, 50%–large dash, 75%–small dash) when inflated to structural failure. Curves exhibit the typical non-linear J-shaped stress-strain relationship of many pliant biological materials. The alimentary tissues are highly extensible under low pressures and then become increasingly stiff with increasing pressure, and the 25% position is overall more extensible compared to the two more distal positions. Asterisk denotes the location where failure always occurred, at the 25% position, providing an estimate of the ultimate material properties (i.e., breaking stress, breaking strain). Tissue from the 50% and 75% positions remained intact, which may underestimate ultimate material properties at these locales.

Fig. 5

Outer radius (A), wall thickness (B), and relative radial percent thickness (C) at three relative positions (25, 50, and 75%) along the length of the alimentary tract, measured from histological cross-sections. Bars are means ± SE, n = 10 for each position. There were no significant differences among groups (Tukey HSD, P<0.05).

Fig. 6

Summary of mechanical properties at three relative positions (25%, 50%, 75%) along the length of the alimentary tract when inflated to structural failure. All values are mean ± SE, n = 10 for each position. (A) Maximal stress, (B) maximal strain, (C) mid-wall extension ratio (λ), and (D) toughness. Different letter above bars indicate signicant differences among group (Tukey HSD, P<0.05). Asterisk denotes ultimate value where structural failure occurred (25% position) from maximal values where the tissue remained intact (50% and 75% positions).

Fig. 7

Strain ratio at three relative positions (25%, 50%, 75%) along the length of the alimentary tract at structural failure. All values are mean ± SE, n = 10 for each position. Asterisk denotes ultimate value where structural failure occurred (25% position) from maximal values where the tissue remained intact (50% and 75% positions). All values are substantially higher than the null strain ratio of 2 (dashed line) for a standard isotropic cylinder, which indicates the extended gut is a non-uniform anisotropic material that is reinforced in the longitudinal direction (Gosline 2018).