1. Lecture 18 Teeth Ruminants Lysozymes and molecular homoplasy Hind-gut fermenters Hard ticks smell cow burps

2. Gary Larson cowphiliac

3. Ennos page 214 Defenses of leaves There are more than 5000 spp. of grass covering >30% dry land: successful. Basal meristem: leaves of grass grow from their base – even if the top of the stem is eaten they can survive. Reinforcement of the leaves comes from fibres (woody sclerenchyma fibres) running longitudinally along the leaf. Lateral cracks are stopped when they reach a new fibre “just as in composite material”. Herbivores have trouble ‘snipping’. Some grasses use SILICA (glass) as a defense. “incorporation of silica bodies, effectively small lumps of glass, into the epidermis of the leaf”. Horses and grasses arms race: hypsodont teeth vs silica abrasion.

4. Selenodont teeth are typical of even-toed ungulates such as deer (Cervidae) and cattle (Bovidae); the cusp’s enamel cutting surface is increased by elongation into a crescent shape. [Selene (moon goddess): major cusp has a half-moon shape.] High-crowned teeth, hypsodont of horses, simply means lots of tooth protruding above the gumline; low crowned teeth have less crown: selenodont teeth are low crowned. Brachydont teeth are the opposite of hypsodont: human teeth are brachydont, i.e., low-crowned. Selenodont teeth are adapted for grinding and the occlusal surface is not covered in enamel (as e.g., in humans); rather, the layers of enamel, dentine, and cement are all exposed, with alternating layers of enamel and dentine wearing unevenly to create an enamel cutting edge. [for further detail: Univ. of Michigan, The Animal Diversity Web]

5. Function of cheek teeth in ruminants Cheek teeth are premolars and molars used to masticate (ten $ word for ‘chew’) and triturate (grind or chew thoroughly). Chewing reduces food to a pulp by compression and shear forces. The lower jaw describes a small circle, pushing mandible teeth up against the maxilla and then shearing them laterally The tooth crowns wear unevenly because of the greater hardness of enamel. Mastication is not the same thing as maceration: maceration means to soften and separate food parts by the addition of a solvent, in this case saliva. Ruminants produce large quantities of saliva: 100-150 litres per day! (R. Bowen) yakkhapadma

6. Treeless grasslands spread across much of the world by the end of the Miocene. Evolving ruminant ungulate mammals exploited prairie grasses as a source of food. Grasslands National Park Saskatchewan

7. Order Perissodactyla are odd-toed ungulates: horses, zebras, tapirs, rhinos. Order Artiodactyla are even-toed ungulates. Artiodactyls include about 180 species: pigs, camels, hippos, deer, giraffes, sheep, cattle, antelopes, goats, bison, musk ox, caribou. Suborder Ruminantia, a suborder of Artiodactyla, comprises the deer family (Cervidae) and cattle, sheep and antelopes (Bovidae); these are the most recently evolved ungulate group; they all have a fully developed 4-chamber stomachs. They have lost the upper incisors and often the canines and have selenodont molars. Some Taxonomy

8. Cellulose: a problem to chew, a problem to digest. Evolving hoofed mammals needed other organisms to access the sugars. Most multicellular animals cannot synthesize cellulases: only micro-organisms can make the necessary enzymes. And the grasses evolved other protections as well, building silica into their wall tissue, a hard crystalline mineral that abrades teeth quickly.

9. Digestive tract of the cow viewed from the right side; the cardia is a weak valve where the oesophagus enters the rumenoreticulum; the whole of the rumenoreticulum is a diverticulum of the gut – a huge fermentation vat for microbes. The omasum connects to the abomasum or true stomach; the pylorus (valve) separates this from the small intestine. Within the rumen ingested plant material separates into three zones: gas produced by microbes rises to occupy the upper regions (methane and carbon dioxide); yesterday’s hay sinks to the bottom, and newly arrived roughage floats in a middle layer.; Diverticulae and valves

10. Guts are muscle-invested tubes organized into a linear sequence of chambers, separated by valves, with sidebranching blind-ending diverticulae. Valves control speed of travel of the ‘disassembly line’. The muscular walls engage in peristalsis and churning to mix the digestant. The rumen and reticulum are an example of a (very large) blindly ending sidebranch of the cow gut; oesophagus empties into the rumen which is semiseparated from the reticulum by a low rumino- reticuluar fold. Grass is ingested by ruminants without chewing, going down the oesophagus past the cardia (valvular entrance into the stomach) and into the rumen. Later this unchewed material moves forward into the reticulum and is formed there into a bolus, this facilitated by the reticulum’s rough walls. The cow regurgitates this bolus into its mouth and chews, i.e. RUMINATES. Rumen and reticulum are eccentric, located toward the cow’s left side. The oesophageal groove/reticular groove runs in the wall of the reticulum and ends at the reticulo-omasal opening leading into the omasum. It is a special kind of valve functioning as a shunt. Ruminoreticular fold High-risk Ingestion is separated in time from chewing, permitting chewing when risk is low.

11. Tripe: lining of the reticulum, criss-crossing ridges and pits, functions in forming the grass/hay boluses that return to the mouth for further chewing; see the oesophageal groove. ideasinfood.com rumenHealth.com College of Veterinary Medicine Univ. of Minnesota The oesophageal groove functions as a shunt. Reswallowed food material can reach the omasum via this groove. The groove is formed by two heavy, muscular folds in the reticulum wall; these can close to create a passage and this passage redirects materials to the reticulo- omasal opening. If the lips remain open the material goes into the rumen. shunt

12. Fistula: opening in the animal’s side giving access to rumen contents for study Cooperative extension system

13. Food is ingested (while exposed to prairie predators) and swallowed quickly into the rumen. The rumen houses bacteria, ciliate protozoa, fungi – micro- organisms with capacity to make cellulases. Rumen content is maintained at a steady pH and constant temperature – ideal conditions for anerobic fermentation. Saliva adds water and mineral ions, e.g, bicarbonate, to this fermentation vat, the latter helping to buffer the contents to maintain the best pH for the microbes. Some nutrient absorption does occur in the rumen via the epithelium of the papillae in its walls. In the rumen micro-organisms digest the carbohydrates of plant cell walls. Carbohydrates both structural (cellulose cell walls) and sugars and starches, when they undergo microbial fermentation produce volatile fatty acids (VFA): e.g., acetic, propionic, butyric etc. The vast majority of VFAs are passively absorbed through the rumen wall. (So while the saliva buffers the pH up, digestion is producing acids moving the pH down; absorption of acids of course shifts the pH up. The rumen microbes also synthesize protein and rumen-living bacteria can use ammonia as a source of nitrogen to make the protein (this is the basis of being able to add urea as a supplement to cattle feed). To gain this protein which is part of the bacteria, the cow must pass the microbes on into the abomasum and digest them. It then treats the protein in a more ‘normal’ nonruminant fashion: absorption within the small intestine.

14. Significance of ruminant adaptation Adaptations ‘explain themselves’ when studied in the context of animal behaviour and ecology and they occur within ‘adaptive systems’. Animal herbivores that evolved fermentation chambers to exploit micro-organism enzyme systems also have selenodont grinding teeth to mechanically break down cellulose cell walls. And they have cursorial (running) adaptations: lengthened legs, extrinsic muscles, hooves adapted for fast running. Limb structures have been selected for good distance advantage at the expense of poor force advantage so hooves can move relatively fast. They have good binocular vision and high sensitivity to objects moving at a great distance in their field of view. There is an integrated package of different adaptations – a system -- explained by a way of life.

15. National Geographic Wallaby: cud-chewing ruminant and a marsupial that evolved its rumination separately from the artiodactyls: like cervids and bovids though, green plant tissue, eaten in haste, is regurgitated in leisure and masticated (chewed) further.

16. Similar stomach chamber features, including an oesophageal groove/shunt evolved in wallabies independently of the evolutionary events that led to the rumen of a cow.

17. Kangaroos & wallabies (Setonix): An example of homoplasy [convergence]: independent adaptation resulting from similar selection processes (think also bat hairs and bee hairs). Stomach diagram illustrates the basis of the oesophageal groove of a wallaby. When the muscular folds are drawn together a separate tube is created which permits chewed material to be reswallowed and to skip chamber 1.

18. Exploiting the digestive capacities of micro-organisms for herbivory The trouble with herbivory is cellulose. Mammals lack the necessary enzymes to deal with the cellulose of plant cell walls. Ungulates evolved a chambered stomach housing ciliate protozoa, yeasts and other micro-organisms which are able to digest cellulose. This ruminant structural adaptation is a fermentation vat diverticulum of the gut, housing unicellular creatures optimally [giving them an ideal habitat]; the mammal exploits the digestive capacities of the micro-organisms. When these have made more of themselves the ungulate passes them further along its gut, kills and digests the micro-organisms to nutritive benefit.

19. Langur monkeys offer another good example of homoplasy. Langurs are monkeys that feed on the leaves of trees. They have an anterior gut chamber that houses bacteria that can break down cellulose. They cannot be called ‘ruminants’ as they don’t chew a cud. But they are obligate herbivores lacking cellulases that benefitted from digesting cellulose.

20. Stewart C-B., Schilling J.W., Wilson A.C. 1987. Adaptive evolution in the stomach lysozymes of foregut fermenters. Nature 330: 401-404. An example of adaptive evolution at the protein (sequencing) level. Lysozymes are special enzymes evolved by animals to deal with bacteria that invade the body. In the gut of mammals there are typical lysozymes that keep the bacterial fauna in the gut space under control: the old function of the lysozyme: lysozymes throughout the body fight invading bacteria (present in tears for example). In two separate lineages, a new function arose independently as a gut lysozyme was recruited to deal with digesting the bacteria progressing onward into the stomach. The ruminant ungulate lineage and the line leading to colebus monkeys: lysozyme was recruited to a new function that of digesting the bacteria that enter the stomach from the fermentation region – these lysozymes are specialized to deal with the higher pH of the stomach. Amino acid sequence of langur stomach lysozyme compared to that of cow: 130 amino acids: the resulting unusual similarity attests to homoplasy.

21. Ixodes ricinus European Sheep tick: vector of Lyme disease, tick-bourne encephalitis, no eyes, 3 mammalian hosts in life cycle Wikki Donze G. Rumen metabolites serve ticks to exploit large mammals. J. exp. Biol. 207: 4283- Hard ticks react to volatile rumen end-products – short-chain carboxylic acids (acetic, proprionic, butanoric etc.) in ‘cow burps’: eructions.

22. The hoatzin, living in mangrove swamps of the Amazon drainage, is the only known foregut fermenting bird.

23. Like cattle, hInd-gut herbivore fermenters* have a chamber of micro-organisms protozoa, bacteria, exploited to break down vegetable matter; this chamber occurs later in the digestive tract. Horses and rabbits use a modified caecum, part of the large intestine. Since this occurs after the absorptive region of the small intestine, the material must be re-eaten: caecotrophy is when food is passed twice through the gut. Hindgut fermentation *horses rabbits rodents like beavers and porcupines

24. Vispo C., Hume I.D. 1995. The digestive tract and digestive function in the North American porcupine and beaver. Can. J. of Zoology 73: 967-974. In the beaver the caecum and proximal colon function together as a fermentation chamber. In the porcupine fermentation is confined to the caecum.