Introduction

Raptors or birds of prey are a diverse group that include owls, falcons, eagles, hawks, kites, and vultures (Fig 1).

Figure 1. The group known as raptors or birds or prey are a diverse group. Photo credits: Dr. Elizabeth Daut (left), Beka Weiss via Flickr Creative Commons (FCC) (middle), and John Haslam via FCC (right). Click image to enlarge.

All raptors consume a meat-based diet ranging from the specialist diet of the fish-eating osprey (Pandion haliaetus) to a generalist diet that can include insects, mammals, birds, reptiles, amphibians, and even carrion. Other than poultry, the exact nutritional requirements of birds are unknown, however the natural raptor diet is always relatively high in protein and fat and low in carbohydrates. Whole prey diets have a calcium/phosphorus ratio of 1.5:1 as the bird actually consumes the bones as well as the meat (Kubiak 2012, Bird 1976).

Gastrointestinal specializations of the raptor

The raptor upper gastrointestinal tract differs substantially from that seen in omnivorous and granivorous birds like parrots and chickens.

• Most diurnal raptors possess a spindle-shaped crop that is particularly well developed in vultures. Owls (Order Strigiformes) lack crops, however food can be stored throughout the esophagus (Murray 2014, Klasing 1998, Duke 1997, McLelland 1979).
• The stomach can expand to hold large prey items with the assistance of mucosal ridges on the serosal surface of the proventriculus. The ventriculus is thin-walled and poorly muscled particularly in comparison to granivorous birds that use the ventriculus to grind seeds and grains (Murray 2014, Denbow 2000, Duke 1997, McLelland 1979).
• Indigestible material, like fur, feathers, and bones, are retained within the ventriculus, compacted into a pellet, and regurgitated or egested (Fig 2) (Forbes 2015, Murray 2014, Duke 1997).
  

  Figure 2. Indigestible material is compacted into pellets or casts in the raptor ventriculus and egested. Photo credit: Dr. Elizabeth Daut. Click image to enlarge.

Evaluation of nutritional status

Body condition scoring

Body condition scoring (BCS) reflects changes in body composition and nutritional status much better than body weight alone. Scoring relies upon palpation of pectoral musculature, visualization of subcutaneous fat stores, and palpation of coelomic fat. The BCS scale in birds is sometimes ranked from 1 (emaciation) to 5 (obesity). Energy excess or obesity is most commonly seen in captive birds housed in permanent breeding aviaries or zoological parks (Forbes 2015, Chitty 2008). Although pectoral musculature can be atrophied from lack of use due to young age or injury, the emaciated patient has typically lost at least one-third of normal body weight and appears abnormally thin (Fig 3).

Emaciation is a common presentation in raptors that have not learned to hunt successfully during their first year. Birds can also present in poor condition due to a variety of causes such as inability to hunt or eat food, inclement weather, chronic injury, or when they become trapped in a building or some other man-made structure (Murray 2014, Handrich 1993, Garcia-Rodriguez 1987, Shapiro 1981). Energy deficits can also be observed in falconry birds as a result of inappropriate training practices (Chitty 2008).

Figure 3. Emaciation (BCS 1) in a first-year red-tailed hawk (Buteo jamaicensis). Photo credit: Dr. Elizabeth Daut. Click image to enlarge.

Blood work

Delay comprehensive testing until the patient is stable enough to handle the stress of restraint and venipuncture. Initial laboratory tests often include hematology, examination of a blood smear for parasites, total protein, packed cell volume, blood glucose, and ideally creatine kinase, lactate dehydrogenase, aspartate transaminase, and electrolytes. Anemia and hypoproteinemia are common findings in the chronically malnourished bird of prey (Fig 4) (Murray 2014, Redig 2009).

Figure 4. A snowy owl (Bubo scandiacus) rehabilitated at The Wildlife Center of Virginia. Initial testing revealed total protein 0.6 mg/dL, packed cell volume 16% and glucose 101 mg/dL. Photo credit: Dr. Elizabeth Daut. Click image to enlarge.

Normal blood glucose levels can be quite variable in raptors. Levels usually exceed 150 mg/dL (8.33 mmol/L) in healthy birds and can reach as high as 800 mg/dL (44.44 mmol/L) in some smaller species. Seizure activity can be observed if glucose levels fall below 80 mg/dL (4.44 mmol/L). Fortunately blood glucose tends to be maintained within normal limits for a relatively long period in the fasting raptor (O’Donnell 1978).

Ancillary testing

Perform fecal parasite testing (wet mount cytology/flotation), particularly for thin birds. Administer an anthelmintic as needed (Murray 2014). Case history and physical examination findings may also dictate additional diagnostic tests such as radiographs and/or endoscopy.

Metabolic needs during starvation versus stress

Starvation

Starvation is associated with a gradual decrease in the metabolic rate, resulting in hypometabolism. During starvation, the patient attempts to maintain normal blood glucose levels by increasing glycogenolysis and gluconeogenesis, while reducing glycogen stores. When glycogen stores are depleted, muscle and fat are broken down to provide substrate for gluconeogenesis. Starvation eventually affects visceral protein mass and the function of vital organs (Parrish 2005).

Glycogen reserves are usually depleted within 24 hours of fasting in the granivorous bird, however research has shown raptors may be relatively tolerant of acute food deprivation. Despite an average loss of 28% and 26% body mass during 8 and 13 days of fasting respectively, barn owls (Tyto alba) and common buzzards (Buteo buteo) were still able to fly and self-feed when food was reintroduced (Handrich 1993, Garcia-Rodriguez 1987). No significant changes in hematocrit or total protein were seen in the fasting buzzards (Garcia-Rodriguez 1987). In contrast, American kestrels (Falco sparverius) that were deprived of food for 3 days, lost 17 –20% body mass and both metabolism and body temperature decreased. Investigators concluded the kestrels would have died if fasting had lasted 5 days (Shapiro 1981).

Hypermetabolism

During physiologic stress like critical illness, the preferred energy source is lean body mass, resulting in increased body protein catabolism. Energy requirements are increased by 30–50% to sustain tissue repair, inflammatory processes, and immune function. Release of catecholamines, glucagon and glucocorticoids increases the rate of gluconeogenesis and glycogenolysis, further increasing the metabolic rate (Labato 1992). Very little is known about the hypermetabolic state in birds in general or raptors in particular, but these same principles are believed to hold true.

Supportive care

Supportive care for the chronically malnourished or emaciated raptor should include fluid therapy, supplemental heat, and measures to minimize stress. In addition to standard stress reduction measures when hospitalizing special species*, raptors can also be calmed by lightly covering the head with a towel or use of a falconry hood (Fig 5).

Figure 5. Falconry hoods are commonly used to calm birds of prey. Photo credit: Andreas Praefcke via Wikimedia Commons. Click image to enlarge.

*Editor’s note: For additional information visit Basic Husbandry: Hospitalizing Non-Traditional Pets and Exotic ICU: Nursing Care for the Avian Patient.

Fluids

Most patients presented to wildlife centers are at least 5% dehydrated, and many thin or malnourished raptors are up to 12% dehydrated. Normalize hydration status gradually over 24–48 hours, although ongoing losses need to be replaced more rapidly. Visit Fluid Therapy in the Avian Patient for additional information.

Subcutaneous fluids are an effective route of administration for mildly ill patients. Place an intravenous or intraosseous catheter for more debilitated patients, but be mindful of the risk for fluid overload in the hypoproteinemic patient. Supplement patients with thiamine and other B vitamins before and during initial re-feeding (thiamine 1–2 mg/kg SC every 24 hours) (Murray 2014). Maintenance fluid support is often continued for 3–5 days after feeding is initiated. Blood transfusion is also an option for the select critical patient with severe anemia and hypoproteinemia.

Supplemental heat

Hypothermia is very common in debilitated, emaciated raptors. Provide supplemental heat to prevent the bird from expending energy on thermoregulation. Warmed intraosseous or intravenous fluids and a heated intensive care unit can elevate both core and peripheral body temperature.

Indications for nutritional support

Indications for nutritional support range from profound weight loss and anorexia to severe illness or injury (Table 1).

Calculating energy requirements

The basal metabolic rate (BMR) represents the minimum amount of energy or kilocalories (kcal) necessary to maintain the body at rest or the energy to stay alive. An estimate of BMR is based on metabolic scaling where BMR = K (Weight in kg^0.75). The K factor is a theoretical constant for kilocalories used over 24 hours. The K value for non-passerine birds is 78 (Murray 2014).

Maintenance energy requirements (MER) equal BMR plus the energy needed for normal physical activity, digestion, and thermoregulation. MER is estimated as 1.5 x BMR (Forbes 2015, Murray 2014, Kirkwood 1981). Larger birds eat more food but require a significantly smaller percentage of their body mass as daily food intake. (Forbes 2015).

Tube feeding

As long as the patient possesses a functional gastrointestinal tract, enteral nutrition can be started once the patient is warm and adequately hydrated (Murray 2014). Oral electrolyte fluids like Pedialyte (Abbott) are sometimes offered before tube feedings. Avoid solutions rich in glucose as raptors have little glucose in their normal diets, and research indicates glucose solutions can hasten death in debilitated birds of prey (Dobbs 1983). View the algorithm shared by Dr. Scott Ford for a helpful summary of the approach to nutritional support for the bird of prey (Fig 6).

Figure 6. Raptor fluid resuscitation and refeeding algorithm. Click image to enlarge. Source: Dr. Scott Ford. Click here to download a PDF version (112 KB)

* Editor’s note: The European Union has recommended a ban on hetastarch (hydroxyethyl starch or HES) use in human patients and the US Food and Drugs Administration has instituted a ‘black box warning’. These colloids have been associated with acute renal injury and coagulopathy in some septic patients. A recent veterinary study has also found an increased risk of an adverse outcome including death or acute renal injury in dogs with HES therapy (Hayes 2016). Some veterinarians have completely eliminated colloid use in their practices while others select lower molecular weight HES, such as Voluven™ (Hospira) or Vetstarch™ (Abbott Labs).

Tube feeding formulas commonly fed to birds of prey include the intensive care diet Emeraid Carnivore (Emeraid LLC), as well as recovery diets like Carnivore Care (Oxbow), a/d Canine/Feline Critical Care (Hill’s), and Maximum-Calorie (Iams). Divide the patient’s caloric needs by the energy content of the tube feeding formula (calories per ml) to determine the total volume of formula needed daily. Gradually increase the total amount fed daily over at least 2–3 days until the patient is fed MER (Box 1). Debilitated patients are typically fed small volumes of formula by three or four times daily (Murray 2014). In well-trained falconry birds, where restraint is not required, this can be achieved with the use of an esophagostomy tube (Huynh et al 2014).

Although calculation of caloric needs is crucial, feedings must also take estimated crop or stomach volume into account. The initial volume fed should be no more than approximately 1–1.5% of body weight, increasing to 2–3% at the next feeding, and the volume fed should not exceed 5% of body weight (Huynh 2014). When using an esophagostomy tube, a smaller volume not exceeding 1.5% is fed with an increased frequency of administration (N. Forbes, written communication, Sep 2015). Deliver formula via rubber tubing or a metal gavage tube or feeding needle (Fig 7) (Box 2).

Figure 7. Tube feeding a red-tailed hawk (Buteo jamaicensis) with a red rubber catheter. Photo credit: Dr. Elizabeth Daut. Click image to enlarge.

Feeding prey foods

Some ill or injured birds of prey can self-feed upon presentation although meals should not begin until the patient is warm and rehydrated. Adult raptors are normally fed once daily and birds fed whole prey should not be re-fed until they have cast (Forbes 2015). Remove casting material, like fur and feathers, if the bird is in poor condition or if medication is given multiple times daily (Forbes 2015).

Once hydration and electrolyte abnormalities have been resolved and the patient maintains body weight well and appears enthusiastic to eat, gradually make the transition from tube feedings to solid foods. The initial meal for such patients often consists of three to four bite-sized pieces of mice or other whole prey, devoid of fur or feathers and soaked in warm water. If the patient passes stool normally (see monitoring below) and no complications are observed, then the amount of food offered can be increased gradually. Work up to several small meals daily, allowing the crop to empty between feedings. Provided the bird has regained normal body condition, continues to demonstrate a good appetite, and is passing normal feces, gradually introduce indigestible material (Murray 2014). Once the patient is stable, offer the entire prey item, including internal organs, to ensure the diet is nutritionally balanced (Fig 8) (Murray 2014, Klasing 1998). Prey should be of appropriate size so the bird can consume the entire item.

Figure 8. Whole prey items are often first offered as a “chopped plate”. Photo credit: Dr. Elizabeth Daut. Click image to enlarge.

If the meal is not eaten immediately, do not allow the food item to sit out for a long period of time as bacterial proliferation and contamination can occur (Chitty 2008). Ideally the food item should be left out no longer than 30–60 minutes (Chitty 2008), particularly when placed outdoors during warm weather months. If the bird does not begin to self-feed, continue tube feedings, offer solid food later in the day or the next day, or assist feed the patient, as clinical status dictates (Fig 9).

Figure 9. Assist feeding a hawk chopped, moistened pieces of whole prey. Photo credit: Dr. Elizabeth Daut. Click image to enlarge.

Feeding growing birds

When hand feeding juvenile birds, offer small pieces of food at a time using tongs or hemostats. Slightly moisten food items with water and carefully monitor crop emptying. Young vultures can be particularly challenging to hand raise because of their tendency to regurgitate with stress. Chitty (2008) recommends partially pre-digesting food items by first soaking food in a commercial pancreatic supplement for 30 minutes.

Young chicks are unable to egest indigestible material or ‘casting’ and are at risk for proventricular impaction and death (Forbes 2015). Do not feed indigestible material to any chick less than approximately 12 days old. Some species like the merlin (Falco columbarius) should not be fed casting until approximately 20 days of age (Forbes 2015). While whole prey diets have a calcium/phosphorus ratio (Ca:P) equivalent to 1.5:1; meat without bone has a Ca:P ratio of 1:20 (Kubiak 2012, Bird 1976). Like all growing animals, raptor chicks have increased calcium and vitamin D3 requirements and if fed a diet without adequate bone or alternative vitamin/mineral supplementation the chick is at risk for nutritional secondary hyperparathyroidism (Fig 10, Fig 11) (Chitty 2008). Deviation of long bones and multiple folding fractures are common findings in raptors exclusively fed meat-only diets (Kubiak 2012).

Figure 10. Lateral radiographic view of a nestling black vulture (Coragyps atratus) with nutritional secondary hyperparathyroidism or metabolic bone disease. Photo credit: Dr. Dave McRuer, The Wildlfe Center of Virginia. Click image to enlarge.

Figure 11. Ventrodorsal view of a nestling black vulture (Coragyps atratus) with metabolic bone disease. Photo credit: Dr. Dave McRuer, The Wildlfe Center of Virginia. Click image to enlarge.

Prey food options

The best diet for captive birds of prey is one that resembles the natural diet as closely as possible (Murray 2014, Chitty 2008, Cooper 2002). Fortunately most raptors in a rehabilitation setting will readily take any appropriate meat source when their preferred food is unavailable (Murray 2014, Chitty 2008), particularly when the food item is sliced open or skinned. Ospreys are a notable exception and hand feeding is often required in captivity (Murray 2014).

The nutritional composition of whole vertebrate prey is generally complete and fairly constant across different types of prey items although the fat content can vary (Murray 2014, Klasing 1998).

Mammals

Rabbits and rodents are commonly fed in captivity to raptors that feed on mammals. Although relatively expensive, laboratory mice and rats are popular food items. Captive-raised rats and mice tend to be higher in fat and lower in protein than their free-living counterparts (Fig 12) (Murray 2014, Chitty 2008, Crissey 1999, Douglas 1994). To minimize the risk of excessive dietary fat, offer sub-adult rats and mice that weigh approximately 75% of adult weight (N. Forbes, written communication, Sep 2015).

Figure 12. An adequate source of nutrition, mice are commonly fed to captive birds of prey, however laboratory-raised mice tend to be relatively high in fat. Photo credit: Dr. Elizabeth Daut. Click image to enlarge.

Birds

Birds commonly fed in a rehabilitation setting include day-old-chicks (DOC), Coturnix quail, chicken, and turkey (Forbes 2015, Murray 2014, Chitty 2008). Chicks are readily available and relatively inexpensive. Good-quality DOC contain adequate amounts of protein as well as good levels of calcium and fat-soluble vitamins. Unfortunately DOC and other avian-derived diets carry an increased risk of transmitting Salmonella spp. and other infectious agents when compared to mammalian diets. The yolk sac is the primary source of calcium and fat-soluble vitamins, therefore DOC should generally be fed with the yolk sac intact (Chitty 2008, Bird 1976) Unfortunately yolk is also a rich source of cholesterol and chicks with intact yolk sacs should not be fed long term more than twice weekly (N. Forbes, written communication, Sep 2015).

Pigeons and doves should not be fed to raptors, as several infectious agents, including Trichomonas* spp., falcon herpes virus, and tuberculosis can potentially be transmitted (Forbes 2015, Murray 2014, Redig 2009, Cooper 2002).

*Editor’s note: With regards to trichomoniasis, some clinicians report successful reduction or prevention of risk by feeding pigeons and doves that have been frozen and thawed. At this time of this posting, there are no primary references that have actually shown that protozoa are killed after freezing. Additionally in one study T. gallinae was very resistant to damage by freezing and was the only trichomonad that survived freezing and thawing for 6 months even without the aid of glycerol as a protectant (McEntegart 1954).

There is one study by Bailey et al, in which freezing T. gallinae-infected pigeon carcasses for 24h inactivated trichomonads, which might reduce the risk of disease transmission (Bailey et al 2000). Several sources also recommended that the crop, cervical esophagus, and head be removed from frozen and thawed pigeon/dove carcasses prior to feeding to decreasing the risk of transmission, although this practice cannot completely eliminate risk as trichomonads can be present in other tissues in the disease state (Ford 2010, Ford et al 2009, Forbes 2008).

Fish

Wild-caught, fresh whole trout is ideal for fish-eating birds of prey as farmed fish is generally much higher in fat (Chitty 2008). Supplement thawed frozen fish with vitamin B1, as activation of thiaminase will destroy available vitamin (Chitty 2008). Supplement thiamine at 30 mg/kg fish as fed orally every 24–48 hours (Murray 2014, Joseph 2006, Cooper 2002).

Storage and handling of prey items

Maintain all food storage tools and equipment in a hygienic manner (Chitty 2008). Utensils, cutting boards, food containers, tables, and gloves should be properly cleaned and sanitized daily (Crissey 2001). Operations that regularly feed prey items, should maintain refrigerators and freezers dedicated to meat storage (Fig 13) (Crissey 2001).

Figure 13. Store prey food in a freezer dedicated to meat storage. Photo credit: Wildlife Center of Virginia. Click image to enlarge.

Freezing food items

Partially eviscerate killed prey immediately prior to freezing, as bacteria within the gastrointestinal tract are most likely to contaminate the meat. Leave other viscera such as liver, kidney, and heart in place (Chitty 2008). Quickly freeze the carcass to prevent overgrowth of bacteria (Forbes 2015), and store carcasses in a freezer kept between –30 to –18°C (–22 to 0°F) (Crissey 2001, AZA NAG). Temperatures above –9°C (16°F) but below the freezing point can adversely affect food appearance and nutrient content (Crissey 2001). Stored meat can be kept for prolonged periods (i.e. up to a year) in a freezer with temperatures maintained at –23°C (–10°F) or lower. There are no studies reporting shelf-life recommendations for a particular species of whole prey (Crissey 2001), however frozen fish should ideally be kept no longer than 4–6 months (Bernard 1997).

Thawing food items

Freezing tends to break down tissues, making prey food more susceptible to bacterial invasion after thawing (Crissey 2001). Incorrect thawing increases the potential for not only bacterial proliferation, but also nutrient loss, loss of palatability, and lipid peroxidation or rancidity (Crissey 2001). NEVER thaw meat at room temperature (Crissey 2001, Bernard 1997). Use running water to thaw meat only in emergency situations as this method increases nutrient loss. The safest and preferred method for thawing prey foods is use of a clean refrigerator at 2°C–3.5°C (36°F–38°F) over 24 –48 hours (Forbes 2015, Chitty 2008, Crissey 2001, AZA NAG). Relative humidity should be maintained at 85-90% in refrigerated spaces (Crissey 2001). Fresh meat or thawed meat should be used within 24 hours (Crissey 2001). Never thaw, eviscerate, and re-freeze food items.

Monitoring the patient

Careful patient monitoring will allow the amount fed to be adjusted as needed (Dierenfeld 2014). Evaluate body weight and body condition score regularly and carefully observe pellets and droppings closely. Remember that a reduction in pectoral muscle mass can be attributed to reduced activity in the face of an appropriate diet.

Raptor droppings or “mutes” generally consist of dark brown to black feces surrounded by white urates and a small amount of clear urine. Feces may be tan colored in birds fed day-old chicks (Fig 14) (Redig 2009, Joseph 2006). Stool may be more watery when casting material is not fed (Cooper 2002).

Figure 14. A relatively large amount of urine and tan feces produced in a bird fed day-old chicks. Photo credit: Dr. Elizabeth Daut. Click image to enlarge.

The volume, appearance and timing of cast or pellet production vary with the species, the diet, and the individual bird (Fig 2)(Chitty 2008). Owls generally egest one pellet per meal. Hawks or falcons often egest one pellet for every two to three meals, depending on the diet fed, less often with chicks, more often with rodents. Multiple pellets can be produced if the meal is very large (Duke 1996, Duke 1976, Balgooyen 1971). Raptors fed white laboratory mice produce tan-colored pellets, while pellets from free-ranging birds tend to be darker. Fresh pellets may be covered with mucus and occasionally some bile staining on the surface. The normal pellet should be odorless.

Failure to produce a pellet can indicate dysfunction of the gastrointestinal tract. Pellet production can occur within 12–16 hours after feeding (Chitty 2008), however the range can vary widely by species, individual health status, and meal. A healthy adult red-tailed hawk may not cast a pellet for 24–48 hours after a large meal (D. McRuer, written communication, Dec 2015).

Water

Free-ranging raptors acquire most of their daily water needs through their diet, however captive raptors should always have access to fresh drinking water (Forbes 2015, Chitty 2008). Consider removing the water dish before flying a bird to avoid waterlogged feathers (Chitty 2008). Ensure water containers can be easily disinfected (Forbes 2015).

Summary

The raptor gut is a fairly simple system with a poorly developed ventriculus and a relatively underdeveloped large bowel or ceca. Nevertheless the functional raptor gastrointestinal tract is very metabolically demanding, requiring high energy and moisture, due to the formation of compacted indigestible material or pellets. Management of weak, emaciated raptors includes minimizing stress, supplemental heat, fluid therapy, as well as supplementation of thiamine and other B vitamins. Nutritional support should not be started until the patient is warm and hydration/electrolyte deficits have been addressed. Initial diagnostic testing may also need to be postponed if the patient is extremely debilitated. Very weak raptors are often tube fed initially. When the patient is carefully transitioned to solid food, rabbits, rodents like mice and/or rats, day-old chicks, and commercially available Coturnix quail are common food items offered.

References