- The raptor bill plays a role in prehension and sometimes killing. Food is torn from the carcass by the sharp cutting edges or tomia of the bill in Falconidae (falcons and caracaras); owls often gulp down prey whole.
- The tongue has a barbed surface, allowing greater manipulation of food.
- The esophagus is strong and distensible.
- Most diurnal birds of prey possess a well-developed crop or ingluvies.
- Owls lack a true crop and instead there is a fusiform enlargement or widening of the esophagus.
- The stomach is thin-walled and muscular, adapted more for storage than grinding. The proventriculus is relatively large and highly distensible. The ventriculus is often smaller and sac-like.
- Ceca are small, vestigial or absent in diurnal birds of prey, but large and well developed in strigiforms.
- The gastroduodenal contraction sequence in raptors is much simpler than that described in granivores. Peristaltic waves move directly from the proventriculus, through the isthmus, into the ventricles, and finally pass into the duodenum.
- A pellet is a compacted mass of indigestible material such as fur, feathers, grains, bones, teeth, and claws.
- The final phase of gastric digestion in the raptor involves pellet formation within the ventriculus and egestion, also known as “casting”.
Raptors are a diverse group of birds consisting of order Strigiformes or owls and diurnal birds of prey such as falcons, hawks, and eagles (Fig 1). Order Falconiformes, traditionally considered a broadly defined, polyphyletic group, has recently been divided into two orders with only family Falconidae (falcons and caracaras) remaining in Falconiformes. Other diurnal raptors belong to order Accipitriformes (Hacket et al 2008, Livezey 2007).
Although the normal diet of free-living raptors varies considerably among species, all raptors hunt and feed on other animals (Klaphake 2006). Meat and fish-eaters possess unique gastrointestinal characteristics that reflect their predatory lifestyle (McLelland 1979).
Raptors possess a sharp, curved bill that plays a key role in prehension. Although sometime used for the killing blow, the beak may instead be used to damage the central nervous system to prevent escape. The “falcon or tomial tooth” along the upper beak is used to sever the vertebrae in Falconidae (Fig 2) (Murray 2014, Klaphake 2006, Houston and Cooper 1975).
Food is torn from the carcass by the sharp cutting edges or tomia of the upper bill in diurnal raptors (Houston and Cooper 1975). Owls often swallow small prey items whole, filling the lower esophagus and proventriculus before food passes into the ventriculus or gizzard (Joseph 2006).
The raptor skull lacks prokinesis or movement of the upper jaw in relation to the braincase. This lack of cranial kinesis is due to fusion of the frontal and nasal bones (Clipsham 1997).
The raptor tongue has papillae, or distinct, keratinized outgrowths of stratified squamous epithelium, which allow greater food manipulation and rapid swallowing of food items (Hunter and Cooper 1975). The tongue is relatively long with a sharp-ended apex that is often somewhat hard and rough with a distinct, median groove (Fig 3) (King and McLelland1984). As in most avian species, the raptor tongue is non-protrusible and lacks extrinsic musculature (Klaphake 2006).
Like the tongue, the oropharynx is covered with a thick layer of stratified squamous epithelium (Houston and Cooper 1975). Backward-pointing rows of papillae run across the roof and floor of the oral cavity to help direct food aborad during swallowing (Fig 4, Fig 5) (Klaphake 2006). The oral submucosa is quite vascular and contains mucous glands.
The esophagus is highly distensible due to longitudinal folds along the entire mucosal surface and a relatively thick smooth muscle layer (Fig 6) (Shiina et al 2005, Houston and Cooper 1975). The accipitriform esophagus has greater ability to expand when compared to strigiforms. There is a thin, glandular submucosal layer (Houston and Cooper 1975) and an inner mucosal layer of stratified squamous epithelium with a thin layer of keratinization with some desquamated cells (Houston and Cooper 1975). Birds lack true upper and lower esophageal sphincters (Wade 2008). The vagus nerve and celiac plexus innervate the thoracic esophagus (Wade 2008).
Most diurnal birds of prey possess a well-developed crop or ingluvies (Fig 7) (Duke 1997). The crop is particularly well developed in vultures (Klasing 1998), with the exception of the bearded vulture (Gypaetus barbatus), the only vulture species to lack a crop (Houston and Copsey 1994). The histologic structure of the crop is the same as the esophagus (Houston and Cooper 1975). To pass food from crop to stomach, the bird of prey will “put over” by first stretching the head up, then pushing the chin down in a flattening motion, often moving the head far to the side (Klaphake 2006).
Instead of a true crop, many owls possess a fusiform enlargement of the esophagus (Fig 8) (Duke 1997).
Carnivores and piscivores feed on relatively large, soft food items that are fairly simple to digest and therefore the raptor stomach is adapted for storage (Hilton 1999, Klasing 1998). Grossly, the large, tubular proventriculus or glandular stomach merges into the relatively small, sac-like ventriculus or gizzard giving the stomach a pear shape (Fig 9) (Klaphake 2005, Langlois 2003, Denbow 2000, McLelland 1979). The isthmus or intermediate zone is often difficult to identify (Gussekloo 2006, Langlois 2003). The pyloric region leading to the duodenum is located in the cranial portion of the ventriculus (Murray 2014, King and McLelland 1984). The avian stomach is innervated by the vagus nerves as well as the celiac and cranial mesenteric plexi (Wade 2008). The celiac artery supplies blood to the proventriculus and ventriculus (Wade 2008).
Like the esophagus, the proventriculus is also highly distensible due to the presence of longitudinal folds (Fig 10, Fig 11) (McLelland 1979). Gastric gland papillae are also visible on the mucosal surface of the stomach. Although papillae are diffusely distributed in most birds, these structures are arranged in longitudinal tracts in owls (Langlois 2003). The proventricular lining was found to be highly glandular columnar epithelium in the white-backed griffon vulture (Gyps africanus) (Houston and Cooper 1975).
The muscle layers of the proventriculus and ventriculus consist of a thick, inner circular layer and an outer, longitudinal layer (Fig 12) (Wade 2008, Denbow 2000, Duke 1997, McLelland 1979). Ventricular muscle is poorly developed, lacking the distinct thick and thin muscles characteristic of the granivore stomach (Wade 2008, Langlois 2003, Denbow 2000, Duke 1997, McLelland 1979).
The protective cuticle layer or koilin is continuously worn and replaced in family Falconidae (Denbow 2000, McLelland 1979). The koilin is absent in some birds of prey like the white-backed griffon vulture (Fig 13) (Houston and Cooper 1975).
Mechanical digestion of food does not occur at any stage in the raptor gastrointestinal tract. Instead food is broken down entirely by chemical digestion (King and McLelland 1984). Gastric contents range from a pH of 1.0-2.0 in vultures and 2.5-5.0 in barn owls (Tyto alba) and kestrels (Falco tinnunculus) (Duke 1975, Houston and Cooper 1975).
Due to the universal role of the intestines in enzymatic digestion and nutrient absorption, there is less variability in this segment of the avian gastrointestinal tract (Fig 14) (Denbow 2000, Klasing 1998, Duke 1986, King and McLelland 1984). All bird intestines are relatively short when compared to mammals, however carnivorous bird possess a shorter tract when compared to granivores (Denbow 2000, Klasing 1998, Klasing 1998, McLelland 1979). There are some exceptions to this rule of thumb. The American kestrel (Falco sparverius) has a relatively large duodenum and the osprey (Pandion haliaetus) has an extremely long intestinal tract arranged in many small loops.
The duodenal loop is found just distal to the stomach, on the right surface of the ventriculus. In most raptors, the duodenum is U-shaped however in the red kite, kestrel, and peregrine falcon the duodenum is arranged in a snail-like coil.
The pancreas sits between the ascending and descending duodenum, extending about half the length of the duodenal loop in strigiforms and even smaller in diurnal birds of prey (Fig 15) (Klaphake 2006). Several biliary and pancreatic ducts open near the distal end of the ascending duodenum in most avian species (Fig 16) (Wade 2008).
The jejunum and ileum are arranged in a number of narrow U-shaped loops. These loops of bowel are found at the edge of the long dorsal mesentery in the right portion of the coelomic cavity (Wade 2008). The jejunoileum forms a double intestinal spiral in the kestrel and peregrine falcon. The most distal portion of the ileum is arranged into a small supracecal loop in a few raptors, including family Falconidae (King and McLelland 1984, McLelland 1979).
The small intestinal mucosa is raised into villi lined with columnar epithelium containing many goblet cells (Houston and Cooper 1975). These villi are more developed and finger-like in the raptor than in other avian species (Houston and Cooper 1975). The intestinal nerve, which is unique to birds, runs the length of the small and large intestine (Wade 2008). The intestinal nerve is considered analogous to the mammalian prevertebral ganglion and contains both sympathetic and parasympathetic autonomic fibers (Wade 2008). The celiac, cranial mesenteric, and caudal mesenteric arteries provide blood supply to the intestines (Wade 2008).
Ceca arise at the junction of the ileum and rectum (Wade 2008). These structures are absent or rudimentary in diurnal raptors. These lymphoid ceca are short, rounded objects, measuring approximately 4 mm in length, and they play no role in digestion (Fig 17) (Gussekloo 2006).
In contrast, the owl cecum is relatively large and well developed, measuring 4-11 cm long with an enormously expanded distal portion containing goblet cells and secretory glands (Fig 18) (Klasing 1998, Duke 1986, McLelland 1979). The cranial mesenteric and celiac arteries provide the blood supply (Wade 2008). Research has shown that these glandular ceca are important in water conservation in the great horned owl (Bubo virginianus) (Duke et al 1981). Cecal droppings, voided less frequently than rectal feces, are periodically observed in owls. These soft, very dark stools should not be mistaken for diarrhea (Murray 2014, Duke 1986, Duke et al 1976).
Rectum and cloaca
The ileum continues through a muscular sphincter into the relatively short, straight large intestine, which is located at the dorsal wall of the body cavity (Wade 2008, Gussekloo 2006). The rectum then terminates in the coprodeal part of the cloaca. Unlike mammals, the avian rectum has numerous flat villi, very few crypts and few goblet cells. Colonic anti-peristalsis has been observed in raptors and presumably plays an important role in reabsorption of water (King and McLelland 1984).
The caudal mesenteric artery supplies the rectum (Wade 2008). The cloaca is innervated by the intestinal nerve and the cloacal ganglion or plexus, which arises from the pudendal nerve and follows the ureter to the dorsolateral cloaca (Wade 2008).
Normal raptor feces or “mutes” harbor a large variety of bacteria that might be expected from a carnivore including coagulase-negative Staphylococcus, coagulase-positive Staphylococcus, Micrococcus sp., Streptococcus sp., Escherichia sp., and Salmonella spp. (Klaphake 2006, Battisti 1998). The normal flora of vultures also appears to consist largely of Gram-negative rods from family Enterobacteriaceae (Klaphake 2006, Lamberski et al 2003, Battisti 1998) Raptors have also been implicated as potential reservoirs of Campylobacter spp.
Close evaluation of feces can provide valuable clinical information. Normal droppings or “mutes” are typically well formed with a black center surrounded by white urates. Emerald green stools can also be observed when the gastrointestinal tract has been empty a few hours (Murray 2004, Klaphake 2006, Cooper 2002). Feces may be tan or brown and sticky on a diet of day-old chicks with a high yolk content, and feces can appear yellowish and granular if white, fatty meat is consumed (Murray 2014, Joseph 2006). Watery stools can be observed in birds that are not offered adequate casting material (see pellet formation and egestion below) (Murray 2014, Cooper 2002).
The gastroduodenal contraction sequence in raptors is simplified when compared to that described in granivores. Peristaltic waves move from the proventriculus through the isthmus, into the ventricles , before finally passing into the duodenum (Murray 2014, King and McLelland 1984).
Pellet formation and egestion
Pellet formation occurs within the ventriculus. Pellets are a compacted mass of indigestible material like fur, feathers, grains, bones, teeth, scales, and claws. Even chitin is present in the pellets of some birds like the American kestrel (Akaki and Duke 1998, Poole 1989, Murray 2014). When compared to Falconidae, owl pellets contain much more bony material, sometimes even complete skeletons, because owl digestive juices are less acidic than in other birds of prey (Fig 19). Other raptors also tend to pluck their prey to a much larger extent than owls (Murray 2014, Duke et al 1975b).
The initial, brief phase of pellet formation consists of muscular contractions that remove liquid from the indigestible material present within the ventriculus. This is followed by 5 to 6 hours of pellet compaction. Approximately 12 minutes before the pellet is expelled, ventricular contractions increase in frequency and amplitude pushing the pellet into the lower esophagus (Fig 20). From here antiperistaltic waves move the pellet toward the oropharynx. The oral expulsion of the pellet is called egestion or ”casting”. Abdominal muscle contractions and duodenal motility are not involved in this process (Murray 2014, Langlois 2003, Denbow 2000, Duke 1997).
When a raptor is about to produce a pellet, the eyes often close and the bird will be reluctant to fly. In owls, the facial disc narrows or elongates. At the moment of expulsion, the neck stretches up and out, the beak opens, and the pellet simply drops out without any retching or spitting motions (Fig 21, Fig 22).
The fresh pellet is an oval structure that is firm yet elastic, slightly damp, and odorless. The surface of the pellet is normally coated with a thin layer of mucus, and large or hard items are usually wrapped within soft items like fur or feathers. Raptors fed white laboratory mice will produce tan-colored pellets. Pellets egested from free-ranging birds tend to be darker due to fur or feather color (Murray 2014).
It is important to monitor pellet egestion in raptors as failure to produce a pellet can indicate dysfunction of gastrointestinal tract (Murray 2014). The average interval from feeding to egestion in owl species ranges from 10 to 13 hours. The interval averages from 19.5 to 23.5 hours in hawks. Owls produce a pellet with each meal, while hawks may eat more than one meal before casting (Klaphake 2006, Duke et al 1976a). Most casts are egested before midmorning or after killing prey, but before the first feeding of the day (Duke 1980, Duke et al 1976a, Kostuch and Duke 1975).
Even among birds of prey, distinctive differences may be appreciated in the gastrointestinal tract. Birds that utilize a “pursuit” mode require speed and agility to capture prey in flight. These species, such as accipiters (Accipiter spp.), peregrine falcon (Falco peregrinus), and barn owls (Tyto alba), have the lightest gastrointestinal tracts relative to body size. These birds “economize” on the weight of the gastrointestinal tract in favor of well-developed flight muscles. Digestion is relatively rapid due to both reduced gut length and increased flow rate of digesta, therefore these birds are more dependent on highly digestible food (Barton and Houston 1996).
Species that utilize a “foraging” mode, like buteos and tawny owls (Strix aluco), have relatively slow digestion and relatively larger, heavier gastrointestinal tracts (Barton and Houston 1996).
There are distinctive differences in the gastrointestinal anatomy and physiology of carnivores and piscivores. Since carnivores feed on relatively large, soft food items, the raptor stomach is adapted more for storage and is thin-walled, sac-like, and muscular, and when compared to granivores, herbivores, and insectivores, the gastroduodenal contraction sequence is quite straightforward in the raptor. Peristaltic waves move directly from the proventriculus through the isthmus, into the ventricles, and finally pass into the duodenum. All raptors also display a complex, final phase of gastric digestion in which a compacted mass of indigestible material (the pellet) formation and egestion of a compacted mass of indigestible material called the pellet. Egestion, also known as “casting”, occurs within the ventriculus.