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

Synopsis 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.

[1]  J. Gosline Mechanical Design of Structural Materials in Animals , 2018 .

[2]  I. Tibbetts,et al.  Enzymatic digestion in stomachless fishes: how a simple gut accommodates both herbivory and carnivory , 2011, Journal of Comparative Physiology B.

[3]  A. Ruiz,et al.  Evolution of Herbivory in a Carnivorous Clade of Minnows (Teleostei: Cyprinidae): Effects on Gut Size and Digestive Physiology , 2009, Physiological and Biochemical Zoology.

[4]  A. Mcintyre Feeding and Digestive Functions of Fishes, J.E. Cyrino, D.P. Bureau, B.G. Kapoor (Eds.). Science Publishers, Enfield, NH, USA (2008), 575 pp., Hardback, Price US$88, ISBN: 978-1-57808-375-6 , 2009 .

[5]  Adam P. Summers,et al.  Hard prey, soft jaws and the ontogeny of feeding mechanics in the spotted ratfish Hydrolagus colliei , 2008, Journal of The Royal Society Interface.

[6]  M. Zatoń,et al.  DUROPHAGOUS PREDATION ON MIDDLE JURASSIC MOLLUSCS, AS EVIDENCED FROM SHELL FRAGMENTATION , 2008 .

[7]  M. Grosell,et al.  Intestinal anion exchange in teleost water balance. , 2007, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[8]  C. Wood,et al.  Plasticity of osmoregulatory function in the killifish intestine: drinking rates, salt and water transport, and gene expression after freshwater transfer , 2006, Journal of Experimental Biology.

[9]  Y. Takei,et al.  Identification of two functional guanylin receptors in eel: multiple hormone-receptor system for osmoregulation in fish intestine and kidney. , 2006, General and comparative endocrinology.

[10]  Mason N Dean,et al.  Prey capture behavior and kinematics of the Atlantic cownose ray, Rhinoptera bonasus. , 2006, Zoology.

[11]  C. D. Hulsey Function of a key morphological innovation: fusion of the cichlid pharyngeal jaw , 2006 .

[12]  I. Tibbetts,et al.  Trophic shifts in three subtropical Australian halfbeaks (Teleostei : Hemiramphidae) , 2005 .

[13]  P. Motta,et al.  Analysis of the bite force and mechanical design of the feeding mechanism of the durophagous horn shark Heterodontus francisci , 2005, Journal of Experimental Biology.

[14]  M. Pack,et al.  Intestinal growth and differentiation in zebrafish , 2005, Mechanisms of Development.

[15]  D. Sklan,et al.  Structure and function of the small intestine of the tilapia Oreochromis niloticus×Oreochromis aureus (Teleostei, Cichlidae) , 2004 .

[16]  Takehiro Sato,et al.  Increase of shell-crushing predation recorded in fossil shell fragmentation , 2003, Paleobiology.

[17]  J. Grubich Morphological convergence of pharyngeal jaw structure in durophagous perciform fish , 2003 .

[18]  Masaru Tanaka,et al.  Thyroid Gland Development in a Neotenic Goby (Ice Goby, Leucopsarion petersii) and a Common Goby (Ukigori, Gymnogobius urotaenia) during Early Life Stages , 2003, Zoological science.

[19]  V. Egorov,et al.  Mechanical properties of the human gastrointestinal tract. , 2002, Journal of biomechanics.

[20]  H. Gregersen,et al.  Mechanical Properties and Collagen Content Differ Between Isolated Guinea Pig Duodenum, Jejunum, and Distal Ileum , 1998, Digestive Diseases and Sciences.

[21]  D. E. Hattin Fossilized regurgitate from Smoky Hill Member of Niobrara Chalk (Upper Cretaceous) of Kansas, USA , 1996 .

[22]  D. Kramer,et al.  Intestine length in the fishes of a tropical stream: 1. Ontogenetic allometry , 1995, Environmental Biology of Fishes.

[23]  E. Brainerd Pufferfish inflation: Functional morphology of postcranial structures in Diodon holocanthus (Tetraodontiformes) , 1994, Journal of morphology.

[24]  S. Norton Role of the Gastropod Shell and Operculum in Inhibiting Predation by Fishes , 1988, Science.

[25]  Giorgio Gabella,et al.  The cross-ply arrangement of collagen fibres in the submucosa of the mammalian small intestine , 1987, Cell and Tissue Research.

[26]  R. Ferraris,et al.  Development of the digestive tract of milkfish, Chanos chanos (Forsskal): Histology and histochemistry , 1987 .

[27]  E. M. Williams,et al.  Chloride uptake in freshwater teleosts and its relationship to nitrite uptake and toxicity , 1986, Journal of Comparative Physiology B.

[28]  R. Livingston,et al.  Ontogenetic patterns in diet and feeding morphology in sympatric sparid fishes from seagrass meadows , 1984 .

[29]  P. Lobel Trophic biology of herbivorous reef fishes: alimentary pH and digestive capabilities , 1981 .

[30]  S. Wainwright,et al.  Shark Skin: Function in Locomotion , 1978, Science.

[31]  T. Pietsch The feeding mechanism of Stylephorus chordatus (Teleostei : Lampridiformes) : functional and ecological implications , 1978 .

[32]  G. Burnstock The Morphology of the Gut of the Brown Trout (Salmo trutta) , 1959 .

[33]  R. B. Clark,et al.  Factors Controlling the Change of Shape of Certain Nemertean and Turbellarian Worms , 1958 .

[34]  A. AL-HUSSAINI,et al.  On the functional morphology of the alimentary tract of some fish in relation to differences in their feeding habits; anatomy and histology. , 1949, The Quarterly journal of microscopical science.

[35]  M. Milligan Trichrome stain for formalin-fixed tissue. , 1946, American journal of clinical pathology.

[36]  A. Al-Hussaini The anatomy and histology of the alimentary tract of the bottom‐feeder, Mulloides auriflamma (Forsk.) , 1946, Journal of morphology.

[37]  J. Krafka COMPARATIVE STUDY OF THE HISTO-PHYSICS OF THE AORTA , 1938 .

[38]  D. L. Fox,et al.  THE STRUCTURE AND FUNCTION OF THE GUT IN SURF PERCHES (EMBIOTOCIDÆ) WITH REFERENCE TO THEIR CAROTENOID METABOLISM , 1936 .

[39]  Sophia Mã ¶ ller,et al.  Biomechanics — Mechanical properties of living tissue , 1982 .

[40]  J. Gosline,et al.  Mechanical properties of elastin along the thoracic aorta in the pig. , 2007, Journal of biomechanics.

[41]  W. Kerfoot,et al.  Colonizing Inland Lakes: Consequences of YOY Fish Ingesting the Spiny Cladoceran (Bythotrephes cederstroemi) , 2004 .

[42]  Steven Vogel,et al.  Comparative Biomechanics: Life's Physical World , 2003 .

[43]  W. Raub From the National Institutes of Health. , 1990, JAMA.

[44]  A. Hiltner,et al.  Organization of collagen fibers in the intestine. , 1983, Connective tissue research.

[45]  F. J. Bourne The Mucosal Immune System , 1981, Current Topics in Veterinary Medicine and Animal Science.

[46]  末広 恭雄 A Study on the digestive system and feeding habits of fish , 1942 .