Mechanical Properties of Alimentary Tissues in Teleostean Fishes

Abstract

Fishes are a diverse paraphyletic group that have evolved numerous abilities to occupy a diversity of niches. One successful feeding strategy that has independently evolved in many clades of fishes is commonly known as durophagy—specializing in eating hard prey by crushing protective shells of mollusks and crustaceans, or ingesting whole intact prey. The majority of studies on feeding in fishes have focused heavily on mechanistic and performance analyses of jaw mechanics and prey capture but few studies have examined the effects of ingesting hard or even soft prey on visceral alimentary tissues. Moreover, secondary loss of the stomach in fishes has also occurred independently in approximately 15-20% of extant species, and stomachless fishes must resist mechanical damage from the initial influx of hard prey structures. If the mechanical properties of the intestinal tissues are not able to withstand the varying degree of physical stress caused by the influx of hard structures (e.g. exoskeletal fragments and spines), especially without the aid of a distensible storage, then mechanical damage could lead to premature death. It would therefore be advantageous for the alimentary system to evolve the ability to withstand mechanical stresses acting on the intestinal wall, particularly as prey size and intake increase with body size, in order to maintain its proper function. The main objective of this dissertation is to evaluate the mechanical properties of intestinal tissues in teleost fishes. I address two distinct questions: (1) do tissue properties vary radially and spatially along the length of the alimentary tract? (2) do tissue properties of the alimentary tract differ over ontogeny? I test the hypothesis that the mechanical properties of the alimentary tract will differ along its length and over ontogeny, and predicted that the proximal region of the gut should be the strongest and most extensible in stomachless fishes that lack a storage depot. I used two stomachless species of surfperches (Family: Embiotocidae), Cymatogaster aggregata and Embiotoca lateralis to gain insight into these questions. I developed a custom pressure inflation technique to measure the passive mechanical properties of the intestinal tract. I showed that in Cymatogaster aggregata the mechanical properties differ significantly at three relative positions (25%, 50%, and 75%) along the length of the alimentary tract, with 25–46% greater ultimate strength, strain, extension ratio, and toughness at the proximal (25%) position compared to the more distal (50% and 75%) positions. I also found find that the alimentary tissues are highly extensible and anisotropic, with the proximal (25% position) capable of a radial expansion of 360% percent from the initial state. I next quantified the allometric changes in alimentary morphology and mechanical properties of the striped perch, Embiotoca lateralis, at three relative positions along the intestinal tract in fish ranging from 4-22 cm in length. My results showed that gut mass and length grow isometrically whereas fish mass, gape area, outer gut circumference and gut wall thickness showed positive allometric growth relative to body length. The mechanical properties changed along the intestinal tract and were 5% stronger, 34% more extensible and 29% tougher at the proximal (25%) position of the intestine compared to the more distal (75%) position. Tissues in fish within large and medium size classes were similar and were 18% stronger, 20% tougher, and 49% more extensible than small size classes. These studies provide insight into the mechanistic and developmental variations in mechanical properties along the gastrointestinal tract and over ontogeny. My results also corroborate the suggestion that the proximal section of the intestinal tract acts as a “stomach” in these agastric fishes. These data contribute to our knowledge of the mechanical properties of alimentary tissues and guide future studies of factors that may not only influence possible selective pressures driving the evolution of intestinal tissues but also the evolution of teleostean fishes.