Nutrition of Birds in the Order Psittaciformes: a Review Elizabeth A

Journal of Avian Medicine and Surgery 15(4):257±275, 2001 ᭧ 2001 by the Association of Avian Veterinarians

Review Article

Nutrition of Birds in the Order Psittaciformes: A Review Elizabeth A. Koutsos, MS, Kevin D. Matson, MS, and Kirk C. Klasing, MS, PhD

Abstract: Over 350 species of birds make up the order Psittaciformes; many of these are maintained in captive environments. Malnutrition is commonly diagnosed in captive psittacine birds; therefore, providing nutritionally adequate diets must be a primary concern. This review integrates quantitative information on the dietary habits and nutritional requirements of psittacine birds to facilitate the formulation and evaluation of diets for birds in captivity. Initially, characterization of the diet and feeding strategy of a particular species in the wild can provide insight into appropriate diet choices in captivity. Knowledge of the gastrointestinal anatomy and physiology can be used to elucidate the capacity of that species to utilize various feedstuffs. For example, the presence of a highly muscularized gizzard may allow a bird to utilize a seed-based diet, whereas a species pos- sessing a small gizzard may be unable to process such a diet. Finally, nutrient requirements determined in a particular species or a related species (eg, similar digestive physiology and feeding strategy) may be applied to create a nutritionally adequate diet. Understanding the factors involved in selecting appropriate diets enables aviculturists, veterinarians, and nutritionists to maintain and propagate these birds with increased success. Key words: nutrition, requirements, diets, avian, psittacine, Psittaciformes

Introduction ments that were scienti®cally determined for poultry were adopted, at least in part, as standards for The order Psittaciformes has 2 families, the Ca- diets of captive psittacine birds. We are now in a catuidae with 21 species (including cockatoos, third phase in which research populations of easily cockatiels, and corellas) and the Psittacidae with propagated species, such as budgerigars (Melopsit- 331 species (including lories, lorikeets, parrots, tacus undulatus) and cockatiels (Nymphicus hol- macaws, parakeets, parrolets, rosellas, and love- landicus), are being used to investigate dietary birds).1 These species are found primarily in many preferences, nutrient requirements, and metabolic tropical and subtropical environments around the capabilities. world, as well as in temperate climates in New The goal of this review is to integrate known Zealand and southern Australia. Many of these quantitative information on the dietary needs of species are kept in captivity as companions and psittacine birds so the diets of captive birds can display specimens and for conservation purposes. be formulated and evaluated. Because the require- Proper nutrition of psittacine birds is essential, and ments for only a few of the more than 40 required malnutrition is one of the most clinically relevant nutrients have been determined in psittacine birds, health issues.2,3 In fact, many commonly fed cap- we will likely be dependent upon the known re- tive diets are de®cient in 1 or more essential nu- quirements of poultry6 for many years to come. trients.4,5 Extrapolations of requirements developed in 1 The evolution of nutrition for psittacine birds avian species to other species should be based on has followed 3 stages. Early diets were based upon the gastrointestinal morphology of the target spe- food habits of wild birds. Next, nutrient require- cies, the diet specializations of free-living mem- bers of that species, and experience gained by avi- From the Department of Animal Science, University of Cal- ifornia, Davis, CA 95616, USA (Koutsos, Klasing); and the De- culturists and veterinarians. These latter 2 areas partment of Biology, University of Missouri, Saint Louis, MO have been summarized in several excellent re- 63121-4499, USA (Matson). views.7±14

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Nutritional Ecology and Diets of Wild vations and gastrointestinal tract contents, the Psittacine Birds glossy black-cockatoo (Calyptorhynchus lathami halmaturinus) feeds almost entirely on seeds of a The dietary feeding strategy of an animal (ie, the single species of native tree (Allocasuarina verti- type of food consumed in the wild) is a valuable cillata), the forest red-tailed black cockatoo (Calyp- nutritional tool used to classify groups of animals. torhynchus banksii naso) eats the seeds of only 2 In general, most birds in the order Psittaciformes native trees (Corymbia calophylla and Eucalyptus consume plant-based diets, and they are classi®ed marginata),27,32 and the vulturine parrot (Psittrichas as ¯orivores. Within this general category, further fulgidus) is a specialized frugivore that consumes subclassi®cations can be made on the basis of the the fruit of only 1 or 2 of the 38 extant species of primary types of parts of plants consumed. Com- ®gs (Ficus species) in its native New Guinea.33 Fi- mon psittacine subclassi®cations include granivory nally, the amount of time spent foraging and/or (grain or seed-based diet, including budgerigars and feeding per day varies depending on the species be- cockatiels), frugivory (fruit-based diet, including ing considered. In general, parrots actively feed in many macaws), and nectarivory (nectar-based diet, 2 sessionsÐ1 in the morning and 1 in the even- including lorikeets and lories).15 Within the category ing.20,27,30 One species, the forest red-tailed black of granivorous birds, smaller birds tend to select cockatoo, was reported to eat not in 2 distinct bouts grass seeds and larger birds tend to select increased but in 1 long daily feeding period.34 In many spe- proportions of seeds from shrubs, which contain cies, including the kaka (Nestor meridionalis sep- higher levels of protein.16,17 tentrionalis), paci®c parakeet (Aratinga strenua), In contrast to birds that specialize on 1 speci®c and ground parrot (Pezoporus wallicus), foraging feed type, many psittacine birds consume more di- and feeding represent the majority (Ͼ 50%) of daily verse diets, including foodstuffs from 2 or more cat- activities.23,25,35 egories. Frugivorous-granivorous psittacine birds are commonly described and include the red-fronted Functional Digestive Anatomy macaw (Ara rubrogenys), regent's parrot (Polytelis anthopeplus), and scarlet macaw (Ara macao).18±20 The digestive anatomy of an animal generally re- Species commonly considered nectarivores, such as ¯ects the type of diet it consumes, and the feeding the rainbow lorikeet (Trichoglossus haematodus) strategies of psittacine species (granivory, frugivo- and Stephen's lory (Vini stepheni), often feed on ry, nectarivory, and omnivory) are re¯ected in these other dietary items, including fruits, seeds, and in- birds' gastrointestinal morphology. sects.21,22 Finally, many psittacine birds eat a large Psittacine digestive tracts (GI tract), like those of variety of ingredients that include animal matter and other avian species, begin at the beak, followed by are best categorized as omnivorous (including many a toothless mouth, tongue, pharynx, esophagus, cockatoos and parakeet species). Psittaciformes crop, proventriculus, gizzard, intestine, rectum, clo- classi®cations by feeding strategy and common diet aca, and vent.15,36±38 Accessory organs include the ingredients are listed in Table 1. biliary and salivary systems, pancreas, intestinal Whereas dietary classi®cations can be made from lymphoreticular tissue, and bursa. Each portion of observations of feeding behavior in the wild, diet the digestive tract provides function for acquiring, ingredients selected by psittacine birds have been digesting, and absorbing nutrients or for immuno- shown to vary over time depending on nutrient competence.15 availability23,24 and sex of the bird23 and between Acquisition of food is enabled by the beak, age classes.25 Another important distinction in se- tongue, and oral cavity. In addition, the psittacine lection of foodstuffs by these birds is their ability beak is used for preening feathers, climbing, court- to adapt to and exploit introduced, nonnative, or ship, parental behavior, and defense.36 Beak shape domesticated sources of food. The budgerigar, cock- and size are often adapted to accommodate pre- atiel, rose-ringed parakeet (Psittacula krameri), red- ferred foods, allowing for more ef®cient use of the fronted macaw, regent's parrot, golden parakeet (Ar- beak. For example, granivorous birds often have de- atinga guarouba), kakapo (Strigops habroptilus), ®ned ridges on the edges of their beaks that are used and hooded parrot (Psephotus dissimilis)19,20,26±31 for seed cracking,39 and an articulation of the max- have been reported to eat nonnative plant matter, illary beak to the skull permits increased gape di- most commonly from grain crops and introduced ameter and absorption of the shock from cracking ornamentals and fruit trees. In contrast, some psit- the hull of seeds. tacine birds are very speci®c about the foods they The tongues of psittacine birds contain a medial consume in the wild. On the basis of ®eld obser- groove from the glottis to the tip40 and have a well- KOUTSOS ET ALÐNUTRITION OF PSITTACINE BIRDS 259

Table 1. Feeding strategies and common diet ingredients of wild birds in the order Psittaciformes.

Feeding Time Species name strategy Common diet ingredientsa spent feedingb Reference Blue and gold macaw ¯orivore seeds, fruits, nuts NR 18 (Ara ararauna) Kaka ¯orivore 1Њ insects, seeds, nectar/pollen, fruit, Ͼ50% of 23 (Nestor meridionalis septentrionalis) sap day foraging Kakapo ¯orivore 1Њ leaves, also mosses, rhizomes, NR 31 (Strigops habroptilus) roots, bark, fruit Military macaw ¯orivore seeds, nuts, berries, fruits NR 18 (Ara militaris) Paci®c parakeet ¯orivore fruits, seeds, ¯owers (dry season); 6±18 h/d 35 (Aratinga strenua) grains, fruits (wet) Red-faced parrot ¯orivore ¯owers, berries, shoots, seeds, seed NR 115 (Hapalopsittaca pyrrhops) pods Scaly-headed parrot ¯orivore seeds (70%), ¯owers (20%), grain NR 116 (Pionus maximiliani) (8%), fruit pulp (2%) Blue-throated macaw frugivore palm fruit, nuts, milk NR 18 (Ara glaucogularis) Buffon's macaw frugivore fruits, ¯owers NR 18 (Ara ambigua) Golden parakeet frugivore fruits, buds, ¯owers NR 29 (Aratinga guarouba) Green-winged macaw frugivore fruits (Hymenaea), palm nuts, seeds NR 18 (Ara chloroptera) Orange-winged amazon frugivore fruit (85% from palm fruit) NR 117 (Amazona amazonica) Red-bellied macaw frugivore fruit (96% from palm fruit, ¯owers, NR 117 (Ara manilata) seed pods Vulturine parrot frugivore 1 or 2 of the 38 extant species of NR 33 (Psittrichas fulgidus) ®gs (Ficus species) Red-fronted macaw frugivore- fruits, seeds 1±4 h/d 20 (Ara rubrogenys) granivore Regent's parrot frugivore- fruit, seeds NR 19 (Polytelis anthopeplus) granivore Scarlet macaw frugivore- fruits, nuts, bark, leaves, shoots NR 18 (Ara macao) granivore Baudin's cockatoo granivore seedsÐ1Њ from nuts of marri (C NR 118 (Cacatua baudinii) calophylla) Budgerigar granivore seeds NR 26 (Melopsittacus undulatus) Carnaby's cockatoo granivore seeds (especially from cones and NR 118 (Calyptorhynchus funereus latirostris) nuts of Proteaceae) Cockatiel granivore seeds (prefers soft, young over ma- 3 h/d 27 (Nymphicus hollandicus) ture, hard seeds) Forest red-tailed cockatoo granivore seeds of two native trees (C calo- 10±12 h/d 34 (Calyptorhynchus banksii naso) phylla and E marginata) Glossy black cockatoo granivore seeds of a single native tree (A ver- 6.4±11 h/d 32, 119 (Calyptorhynchus lathami halmaturi- ticillata) nus) Ground parrot granivore seeds, some insect larvae most of the 25 (Pezoporus wallicus) day Hyacinth macaw granivore palm nuts (50% lipid content) NR 18 (Anodorhynchus hyacinthinus) Lear's macaw granivore 1Њ palm nuts, fruit NR 18 (Anodorhynchus leari) 260 JOURNAL OF AVIAN MEDICINE AND SURGERY

Table 1. Continued.

Feeding Time Species name strategy Common diet ingredientsa spent feedingb Reference Pale-headed rosella granivore seeds (3±73%), animal matter (0± NR 120 (Playcerus adscitus) 26%) (varies with season) Red-fronted macaw granivore nuts, seeds, fruit NR 18 (Ara rubrogenys) Red-tailed black cockatoo granivore seeds NR 18 (Calyptorhynchus magni®cus samueli) Rose-ringed parakeet granivore seeds NR 28, 121 (Psittacula krameri) Spix's macaw granivore palm nuts NR 18 (Cyanopsitta spixii) Palm cockatoo granivore- seeds, fruit, seeds from fruits eaten NR 122 (Probosciger terrimus) frugivore by cassowaries Rainbow lorikeet nectarivore 1Њ nector, pollen, fruits, seeds NR 22 (Trichoglossus haematodus) Stephen's lory nectarivore nectar, pollen, fruit, insects (1Њ lepi- NR 21 (Vini stepheni) dopteran larvae) Corella omnivore 1Њ grains and seeds (up to 80%), NR 123, 124 (Cacatua pastinator) some insect larvae Eastern rosella omnivore seeds (3±73%, animal matter (0± NR 125 (Platycercus eximius) 50%) (varies with season) Hooded parrot omnivore 1Њ seeds (1Њ sesame), ¯owers, inver- NR 30 (Psephotus dissimilis) tebrates Major Mitchell cockatoo omnivore larvae, fruits, seeds NR 118 (Cacatua leadbeateri) Black cockatoo omnivore 1Њ seeds, fruits, ¯owers, insects/lar- NR 119 (Calyptorhynchus species) vae, pine cones Red-crowned parakeet omnivore 1Њ ¯owers, seeds, also fruit, vegeta- NR 24 (Cyanoramphus novaezelandiae) tion, invertebrates Red-tailed amazon omnivore seed, fruits, ¯owers, leaves, nectar, NR 126 (Amazon brasiliensis) insects Sulphur-crested cockatoo omnivore seeds (1Њ sun¯ower), grubs, rhi- NR 118 (Cacatua galerita) zomes Yellow-crowned parakeet omnivore 1Њ invertebrates, also plant matter NR 24, 127 (Cyanoramphus auriceps auriceps) a 1Њϭprimary. b NR indicates not reported; h/d ϭ hours/day. developed lingual nail, consisting of a stiff cuticle Four general drinking methods have been de- covering of the ventral and lateral surfaces of the scribed42: Cacatuidae (cockatoos), scoop water with tongue.39,41 Furthermore, these birds have special- the lower bill and ¯ush it back with the tongue; ized muscles associated with the lingual nail and Loriinae, lap water with the brush-tipped tongue; apex of the tongue that allow for enhanced ¯exi- Psittacinae, ladle water with the tip of the tongue, bility and food manipulation, complementing the which is then pressed into the palate to move the functions of the hyoid apparatus used by most other water back; Psittrichadinae and Loriculinae, keep birds for tongue mobility.39,42 Slight differences in the tongue pressed against the palate and drink with tongue anatomy may be found between psittacine a suction-pump action. species. For example, species in the subfamily Lo- Touch receptors, which confer strong tactile riinae (lorikeets) consume pollen and nectar from sense, are found in rich supply on the tongue, oral ¯owers and have tongues that are longer and nar- cavity, and beak. In contrast, avian taste buds, found rower than those of granivorous and frugivorous in the oral cavity on the ¯oor of the pharynx and parrots.43 the base of the tongue,44 are found in much lower The ¯exibility and muscularity of the tongue per- numbers than those in mammals. Parrots have been mit its use by psittacine birds to aid in drinking. reported to have 350 taste receptors, compared with KOUTSOS ET ALÐNUTRITION OF PSITTACINE BIRDS 261

9000 in humans.45 These data suggest that birds periods when nectar is unavailable and pollen is the generally have poorer taste acuity than mammals. primary food source.40 Despite the paucity of taste buds, taste has been The proventriculus and gizzard of psittacine birds demonstrated to be an important factor in determin- are variable in their functional anatomy. The pro- ing food acceptance and avoidance for birds. Nec- ventriculus contains gastric glands that produce HCl tarivores differentiate between sugar solutions based and pepsin, which begin to break down and emul- on composition46,47 and concentration.48 Secondary sify foods. In budgerigars, the gastric glands are plant compounds such as tannins prevent some ¯o- coiled and branched tubular complexes served by a rivorous species from eating certain plant food- single duct each.56 The gizzard of granivorous spe- stuffs,49 and common defense secretions of insects cies is large and muscular, with a thick interior ko- are effective in repelling birds at very low concen- ilin lining; nectarivorous species tend to have a trations (1:4000).50 smaller, less developed gizzard.43 Digestion of pol- Recent studies on cockatiels suggest that their len is not thought to require crushing by the giz- gustatory abilities are quite variable and depend on zard,57 and consequently quick passage through this the compound being tested.51,52 For instance, these organ probably does not reduce digestibility. In nec- birds are particularly insensitive to 3 common sug- tarivores, access in and out of the proventriculus ars (sucrose, fructose, glucose), with thresholds and gizzard lies in the same medial plane as the ranging from 0.16 to 0.40 mol/L, but particularly entrance to the duodenum. This arrangement facil- sensitive to representative plant secondary com- itates quick processing of highly digestible nectar pounds (quinine, gramine, and tannins), with thresh- but presumably diminishes the capacity to digest olds ranging from to 0.0001 to 0.01 mol/L (K. D. seeds and hard-bodied insects. M., unpublished data, February 2001). Cockatiels, Once food particles are broken down and par- and other birds, typically reject salts around the tially emulsi®ed, the digesta moves into the small point of osmolarity.51±54 Put in context, the ability intestine. The primary functions of the small intes- of cockatiels to taste quinine nears the threshold of tine are enzymatic digestion and nutrient absorp- humans, whereas the same birds are much less sen- tion.36 Pancreatic enzymes hydrolyze most starches, sitive than humans to fructose. These data concern- proteins, and nucleic acids in foods, but the pro- ing avian gustatory abilities suggest that cockatiels portion of enzymes released during a meal varies are more sensitive to those ``ecologically relevant'' with species.58 The presence of lactase has not been compounds (ie, toxic secondary compounds in the demonstrated, rendering lactose-containing foods case of a granivore, sugars for nectarivores, etc) and indigestible. Nutrient absorption occurs across the less sensitive to those compounds that are unlikely intestinal villi into the enterocytes. By enhancing to be encountered. These studies also suggest that surface area, the villi facilitate nutrient absorption some species may have keener abilities of nutrient in this region. Some frugivorous species and nec- detection, whereas others have sharper toxin avoid- tarivorous species have exceptionally long (7␮m) ance capacities. Recent research indicates that the intestinal microvilli,38 which presumably aids in ab- transduction pathways of some taste receptors are sorption of the free sugars found in their food. Villi plastic and adaptable rather than passive as once extend into the rectum and coprodeum of budgeri- thought. This plasticity may endow these receptor gars but not many other species.56 cells with the ability to regulate taste responses in The ceca of birds in the order Psittaciformes are relation to nutritional status.55 absent or vestigial,59 resulting in little or no hindgut Once food leaves the oral cavity, it enters the fermentation of poorly digestible carbohydrates. esophagus, which is expandable to allow large food Therefore, the small intestine terminates at the rec- items to be swallowed. The esophagus widens into tum, which empties into the cloaca. The cloaca the crop, which consists of a thick, corni®ed epi- serves as a storage site for urine and feces. In many thelium that protects the bird from damage resulting avian species, retrograde movement of urine from from swallowing whole foods. This region allows the cloaca to the rectum allows for resorption of for softening of food to enable more ef®cient di- protein, salts, and water; this phenomenon likely oc- gestion of feedstuffs, as well as regurgitation of curs in psittacine birds as well. softened food to chicks. Crop capacity has been The average length of time that food is retained shown to change seasonally; the crop of the purple- in the GI tract (mean retention time) depends upon crowned lorikeet (Glossopsitta porphyrocephala) food characteristics, feeding strategy, digestive holds almost half of the contents of the entire GI anatomy, and body size. In general, larger birds tract when nectar is highly available, although crop have longer GI tracts and retention times. The rate volume decreases to less than half this size during of passage of digesta in psittacine birds has not been 262 JOURNAL OF AVIAN MEDICINE AND SURGERY well studied. However, across avian nectarivores, amounts described above. For example, budgeri- typical mean retention time is approximately 30±50 gars, which have no requirement for drinking water, minutes (but it is 80 minutes in rainbow lorikeets),60 choose to consume an average of 4 ml water/day.66 whereas in granivores retention times are approxi- There is also considerable individual variation in mately 40±100 minutes, and in frugivores retention water consumption, and polydipsia can be psycho- times are approximately 15±60 minutes.15,61 The genic.67 In our colony at University of California, mean retention time is typically an order of mag- Davis, cockatiels (93 g), which require approxi- nitude shorter than the time required for complete mately 2.5 ml water/d actually consumed an aver- evacuation of the GI tract. Complete evacuation of age of 13.6 ml/d.68 Variation in water intake be- a single meal from the crop of a budgerigar takes tween birds was very high (4.5±31.5 ml/d, coef®- 11.75 hours, whereas complete evacuation of the cient of variation ϭ 51%), although individual birds entire tract takes 26 hours.62 tended to consume similar amounts of water each day (average coef®cient of variation for each bird Nutrient Requirements ϭ 18.6%). Similarly, high variability has also been described in lovebirds and cockatoos.69 Birds con- Water suming fresh fruits and vegetables, which are often Often forgotten, but easily the most critical nu- in excess of 85% water, would be expected to con- trient for most species, water is essential for main- sume much lower than expected levels of drinking tenance of cellular homeostasis, epithelial integrity, water. Clearly this huge variation in water intake food digestion, waste excretion, hygiene, and nu- makes medication or nutrient supplementation via merous metabolic reactions. The exact quantity re- the drinking water ill advised unless accurate infor- quired each day is dependent upon body size, diet, mation on the consumption of individual birds is and environmental temperature. In general, birds known. conserve water very effectively because feathers minimize evaporative losses and excretory losses Energy are low because of the effectiveness of the renal± cloacal complex. In budgerigars at thermoneutral The maintenance energy requirement is the temperatures, about 35% of daily water loss occurs amount of dietary metabolizable energy (ME) need- via excretion and 65% via evaporation.63 Very small ed to support basal metabolism, as expressed by granivorous birds can survive without any drinking basal metabolic rate (BMR), plus additional energy water because they produce suf®cient water meta- to fuel activity and thermoregulation. Growing birds bolically through oxidation of carbohydrate and fats also need energy to support the accretion of new to replace water losses. The budgerigar (27 g) and tissues, reproducing birds need additional energy Bourke's parrot (Neophema bourkii; 39 g) can live for accretion of gametes, and molting birds need without drinking water at cool temperatures (10± energy to support feather growth.15 Obviously, the 20ЊC)64 but require drinking water at higher tem- total energy requirements vary depending upon the peratures. Larger species require a water source at environment, stage of life cycle, and genetics of the all environmental temperatures. MacMillen and individual. Knowledge of energy requirements is Baudinette64 determined the water requirement of very important because they are the primary factor adult parrots (ranging from 48 to 295 g) to be ap- that determines the amount of diet that should be proximately 2.4% of body weight. fed or will be voluntarily consumed.15 As environmental temperatures rise, water re- A large number of studies have examined the quirements increase. Physiologically, this change in BMR of psittacine birds. McNab and Salisbury70 requirements is due to increased water evaporation analyzed available data and concluded that the from the skin and the lungs as the bird cools itself BMR of psittacine birds is dependent upon the ther- by panting. For example, monk parakeets (Myiop- mal climate of the species' origin but is unrelated sitta monachus) housed at 45ЊC have 12 times the to food habits or water availability. Species origi- rate of evaporative water loss compared with birds nating from tropical climates have BMRs similar to housed at 30ЊC.65 Though some evaporative water those of other nonpasserines (BMR [kcal/d] ϭ 73.6 loss is replaced by metabolic water, most must come ϫ body weight [kg]0.73; [kJ/d] ϭ 308 ϫ body weight from drinking water, and the amount of drinking [kg]0.73). Species originating from temperate cli- water consumed would be expected to increase by mates of New Zealand and Australia have a BMR a factor of about 10-fold in very hot weather. that is 21% higher than tropical species. When water is freely available, most birds drink Though research has provided us with accurate considerably more water than the minimum estimates of the BMR of Psittaciformes species, KOUTSOS ET ALÐNUTRITION OF PSITTACINE BIRDS 263

birds expend this level of energy only when sleep- Table 2. Estimation of metabolizable energy require- ing. Even the act of alertly perching increases en- ments for adult birds in the order Psittaciformes from ergy expenditure by about twofold in budgerigars.71 body weight (BW). Other activities like preening, eating, or shuf¯ing locomotion increase energy expenditure by about Energy requirements 2.3-fold over BMR. Flight of budgerigars is espe- Housing conditionsa (kcal/d) (kJ/d) cially expensive and requires 11 to 20 times more Indoor cage 154.6∗BW0.73 647∗BW0.73 energy per minute than BMR.72 Buttemer et al71 Indoor aviary 176.6∗BW0.73 739∗BW0.73 closely observed budgerigars kept in large outdoor Outdoor aviary, summer 203.9∗BW0.73 853∗BW0.73 aviaries (12 ϫ 6 ϫ 4 m). These birds were more Outdoor aviary, winter 226.1∗BW0.73 946∗BW0.73 active in the wintertime than the summertime, but Free living 229.2∗BW0.73 959∗BW0.73 they still spent 94% of their time perching. The re- a Assumptions: birds housed in cages indoors are in thermo- mainder of their activity was associated with preen- neutral zone and ¯y only minimally; birds in aviaries have the ing (35 minutes/day), eating (34 minutes), shuf¯ing opportunity for short ¯ights. equations were derived from pub- around (10 minutes), and ¯ying (5 minutes). In ad- lished estimates of basal metabolic rate (reference 128) and activity cost (references 71, 73) per kg BW. dition to energy required to support activity, thermoregulation requires signi®cant amounts of ener- getic input, primarily at low ambient temperature. Accurate daily energy requirements for captive In the winter (average temperature of 5.9ЊC), daily psittacine birds are available only for budgerigars, energy requirements were 21% higher (24.1 kcal/d; which presents a problem for nutritionists con- [101 kJ/d] or 3.07 times BMR) compared with the cerned with other species. However, there is often summer (20.0 kcal/d [83.8 kJ/d] or 2.77 times a good correlation between daily energy expendi- BMR), when the temperature averaged 20.7ЊC.71 tures and BMR.76,77 Relatively accurate and repre- The thermoneutral zone of winter-adapted budgeri- sentative information on the BMR of Psittaciformes gars ranged from 22 to 35ЊC, and summer-adapted species can be used as a basis to calculate daily birds began to expend additional energy for ther- energy requirements. With this empirical approach, moregulation when the temperature went below the BMR can be calculated for any species of in- 28ЊC. Finally, the energy requirements of free-living terest on the basis of its body weight and the ap- birds are typically greater than those of captive propriate multiplication factor (Table 2). birds because of their extra costs for foraging for The amount of food required to ful®ll the energy food, thermoregulation, and defenses. Williams et requirement is dependent upon the density of me- al73 measured the daily energy expenditure of free- tabolizable energy in that food and its digestibility. living Port Lincoln parrots (Barnardius zonarius) There appears to be a divergence in the digestive and galahs (Cacatua roseicapilla) when nesting and capacity of birds in the order Psittaciformes de- found that their daily ME requirements were 3.0 pending upon their dietary specialization. Granivo- and 3.23 times BMR, respectively. rous and omnivorous species are comparatively ef- The energy requirements for chick growth will ®cient at obtaining energy from foods, whereas nec- be based upon the fractional growth rate of that spe- tarivorous species are relatively inef®cient (Table cies. Birds in the order Psittaciformes are among 3). the slowest growing of altricial species10 and also When provided ad libitum access to food, birds develop endothermy at an earlier age.74 Thus, their generally eat an amount that satis®es their daily en- energy requirements are likely to be more similar ergy expenditure. For example, red lories (Eos bor- to precocial species than to highly altricial species, nea) are able to adjust their intake of nectars that which grow faster and thermoregulate later. Kam- contain variable energy densities so that their daily phues and Wolf75 measured the rate of protein and energy intake is constant.78 Thus, when provided di- lipid gain in growing budgerigars (177 mg/d and ets with lower than normal energy density (eg, high- 160 mg/d, respectively) and lovebirds (153 mg/d ®ber foods), animals increase the grams consumed and 153 mg/d, respectively). Correcting these rates each day, and, conversely, when presented a diet for the cost of deposition (10.8 kcal/g or 52 kJ/g) with high energy density (eg, high-fat foods), they gives the additional energy needed for growth at 3.6 decrease intake. However, the regulation of food in- kcal/g (17.5 kJ/g) for budgerigars and 3.8 kcal/g take is not always perfect, and obesity can result (15.9 kJ/g) for lovebirds. Earle and Clarke66 report- when diets with high energy densities are fed. For ed that the peak energy provisioned to budgerigar budgerigars, a diet containing 13 megajoules (MJ) chicks was maximal about a week before ¯edging of metabolizable energy (ME)/kg results in main- at 6.7 kcal/chick/day (28 kJ/chick/day). tenance of body weight, but diets of 14 MJ/kg or 264 JOURNAL OF AVIAN MEDICINE AND SURGERY

Table 3. Digestibility of diets by adult birds in the order Psittaciformes.

Dry matter GEb MEb Assimilation Species Diet (GE/g) (ME/g) ef®ciency (%) Reference Kaka sun¯ower seeds, small 6.9 kcal/g 5.4 kcal/g 78.9 129 amount of applea (28.8 kJ/g) (22.7 kJ/g) Kaka insect larvae 8.1 kcal/g 7.3 kcal/g 91.16 129 (33.9 kJ/g) (30.6 kJ/g) Rainbow lorikeet bread, honey, dried milka 4.4 kcal/g 3.9 kcal/g 88.9 120 (18.3 kJ/g) (16.3 kJ/g) Budgerigar corn, soybean meala 4.2 kcal/g 3.3 kcal/g 80.0 83 (17.5 kJ/g) (14.0 kJ/g) Budgerigar white millet 4.0 kcal/g 3.7 kcal/g 93.4 66 (16.7 kJ/g) (15.6 kJ/g) Budgerigar red millet 3.7 kcal/g 3.4 kcal/g 92.0 66 (15.5 kJ/g) (14.2 kJ/g) Budgerigar canary seed 3.3 kcal/g 2.9 kcal/g 88.2 66 (14.0 kJ/g) (12.3 kJ/g) a Dietary proportions of each feedstuff not provided. b GE indicates gross energy; ME, metabolizable energy. above resulted in obesity.79 Ad libitum intake rates mine the amino acid requirements of small graniv- reported in the literature are summarized in Table orous psittacine birds at maintenance. In budgeri- 4. gars, 6.8% crude protein (0.33% sulfur amino acids, 0.15% lysine, 14.4 MJ ME/kg) maintained body Protein and amino acids weight,79 but whether or not skeletal muscle mass was maintained is unclear. Underwood et al83 found In general, avian species are unable to synthesize that a corn-based diet containing 12% protein (14.0 the ``essential'' amino acids arginine, isoleucine, MJ ME/kg), but supplemented with lysine (0.29% leucine, lysine, methionine, phenylalanine, valine, methionine cysteine, 0.63% lysine), was adequate tryptophan, and threonine. Glycine, histidine, and ϩ proline are often considered essential on the basis to maintain weight and body composition of adult of research in chickens that demonstrated that rates budgerigars. However, a seed-based diet with 12.8% of synthesis of these amino acids cannot meet met- protein that was low in lysine resulted in increased abolic demands.80 As demonstrated in chickens, a body fat. Because this seed-based diet was also requirement for glycine has been observed for the clearly de®cient in calcium and several trace nutri- budgerigar,81 suggesting that psittacine birds are un- ents, whether the problems with obesity were due able to synthesize enough glycine to meet metabolic to low amino acid levels or to other problems with demands. Furthermore, an essential level of protein a seed-based diet is not clear. In a trial with adult must be included in the diet to meet nitrogen re- male cockatiels, 11% protein (soybean-based diet) quirements of the animal. The quantitative require- supplemented with methionine (0.51% methionine ment for amino acids is dependent upon the phys- ϩ cysteine, 0.77% lysine) was adequate for main- iological state of the bird, being lowest in adults at tenance of body weight and prevention of obesity.68 maintenance and highest in hatchlings and females These experiments indicate that the protein require- laying large clutches of eggs (Table 5). In the wild, ment for cockatiels and budgerigars is probably some psittacine birds time their breeding to the sea- 11% or less if a high-quality protein source is used sonal availability of higher protein foods,82 indicat- or if plant protein is supplemented with the ®rst ing that amino acid nutrition is a major determinant limiting amino acid (the amino acid found in the of reproductive output. In captivity, cockatiels in- lowest proportion compared with dietary require- creased egg lay after protein content of the diet in- ments). When seed protein sources are used, with- creased (E. A. K., unpublished data, February out supplementation, a higher level of protein would 2001). be required. Across granivorous avian species, the For an adult bird in a nonbreeding, nonmolting protein requirement (expressed as percentage of the maintenance state, amino acid and protein require- diet) increases with increased body size15; therefore, ments are related to the rate of obligatory losses.15 higher levels of protein may be required by macaws Several experiments have been conducted to deter- and other larger psittacine birds. Preliminary exper- KOUTSOS ET ALÐNUTRITION OF PSITTACINE BIRDS 265

Table 4. Reported food intake of captive adult birds in the order Psittaciformes.

Intakeb Refer- Species Environment Diet (ME)a (% BW/d) ence Budgerigar colony cages corn/soy meal 25% 83 (Melopsitticus undulatus) (3.3 kcal/g, 140 MJ/kg) Budgerigar colony cages millet, canary grass, oat 26% 83 groats Budgerigar temperature-controlled room Japanese millet 19.6% 62 Budgerigar small cage millet (2.9 kcal/g, 12.13 MJ/ 14% 130 kg) Rainbow lorikeet metabolism cage sucrose/dextrin/egg white 8.4% 86 (Trichoglossus haematodus) (4.0 kcal/g, 16.73 MJ/kg) Rainbow lorikeet small cage bread, honey, dried milk 10.4% 120 (4.4 kcal/g, 18.3 MJ/kg) African grey parrot small enclosure extruded granulesc (2.7 kcal/ 9.8% 112 (Psittacus erithacus) g, 11.5 MJ/kg) Amazon parrots small enclosure extruded granulesc 6.2% 112 (Amazon species) (2.7 kcal/g, 11.5 MJ/g) Lesser crested cockatoo small enclosure extruded granulesc 9.1% 112 (Cacatua sufurea sulfurea) (2.7 kcal/g, 11.5 MJ/g) Blue and gold macaw small enclosure extruded granulesc 7.8% 112 (Ara ararauna) (2.7 kcal/g, 11.5 MJ/kg) a Metabolizable energy (ME) content is based on values for chickens except when ME content of mixed seeds diets cannot be estimated because the proportion of seed consumption was not reported. b Dry matter intake, excluding hulls; BW indicates body weight. c Commercially available extruded granules, unknown composition. iments with African gray parrots (Psittacus eritha- lories, Eos bornea) and frugivorous (Pesquet's par- cus erithacus) suggest a requirement of between 10 rots, Psittrichas fulgidus) species compared with and 15% protein to maintain plasma protein levels.84 granivorous budgerigars,62,85 indicating that their Obligatory nitrogen losses from the gastrointes- protein requirement should also be lower. Frankel tinal tract are relatively low in nectarivorous (red and Avram86 examined dietary protein dynamics in

Table 5. Levels of protein and amino acid shown to be adequate for birds in the order Psittaciformes at a given physiological state.

Protein source Protein Species Physiological state (ME level)a level Reference Budgerigar maintenance puri®ed amino acids (3.4 kcal/g, 6.8% 75 14.4 MJ/kg) Budgerigar maintenance corn (ϩ lysine, 3.4 kcal/g, 14.23 12% 83 MJ/kg) Cockatiel maintenance soybeans (ϩ methionine, 3.5 kcal/g, 11% 68 14.57 MJ/kg) African grey parrot maintenance corn and soybeans; NR 10±15% 84 Rainbow lorikeet maintenance egg white (4.0 kcal/g, 16.65 MJ/kg) 2.9% 86 Budgerigar egg production corn and soybeans (ϩ lysine and 13.2% 89 methionine, 3.2 kcal/g, 13.39 MJ/ kg) Budgerigar growth soybeans (ϩ methionine, 3.2 kcal/g, 13.2% 89 13.39 MJ/kg) Cockatiel growth soybeans (ϩ methionine, 3.5 kcal/g, 20% 90 14.64 MJ/kg) Cockatiel growth puri®ed amino acids (4.0 kcal/g, 0.8% ly- 91 16.74 MJ/kg) sine a ME indicates metabolizable energy; ϩ indicates additive; NR, energy concentration not reported. 266 JOURNAL OF AVIAN MEDICINE AND SURGERY rainbow lorikeets and observed very low rates of 13.2% protein (0.65% lysine, 0.78% methionine ϩ obligatory nitrogen losses. They found that the cysteine, 13.39 MJ ME/kg) supported maximal maintenance protein requirement was only 2.9% growth in growing budgerigar chicks. Neither the when high-quality, readily digestible protein (egg protein nor the amino acid requirement for growth white) was fed. However, the protein in pollen is of other birds in the order Psittaciformes has been considerably less digestible,57 indicating the need determined. for higher dietary protein levels with this food Feathers are a predominant part of the protein source. mass of birds. In budgerigars and lovebirds, they Protein and amino acid requirements for repro- compose 5.7% and 3.5%, respectively, of the body duction are dependent on the number of eggs laid weight, which is 28% and 22% of total body proper clutch, the intensity or frequency of egg laying, tein.92 Most adult birds molt several times a year. and the protein composition of the eggs. The amino This periodic event is associated with increased acid composition of budgerigar eggs is similar to amino acid needs for the synthesis of replacement those of chickens87 and other avian species,88 so feathers and, to a lesser degree, for the synthesis of there is no reason to expect that the appropriate bal- new feather follicles, feather sheaths, and epidermal ance of dietary amino acids should differ markedly blood vessels. The amino acid composition of feath- among species. However, rates of egg production ers is considerably different from other body pro- usually differ between species. Amino acid and proteins or egg proteins. Feathers are enriched in cys- tein requirements are increased most in avian spe- teine and many of the nonessential amino acids, cies that lay on a daily basis and have large clutch- whereas budgerigar feathers contain only 18% as es, whereas the requirements for species that lay a much lysine and 32% as much methionine as the single egg or lay on an intermittent cycle are often carcass.87 Thus, the primary need for feather growth increased only slightly above maintenance require- is cysteine and amino nitrogen. However, whereas ments.15 Budgerigars maintain breeding perfor- feathers grow continuously throughout the day and mance with a 13.2% protein diet (13.39 MJ ME/kg, night, dietary amino acids are supplied only after 0.65% lysine, 0.78% methionine ϩ cysteine) as in- meals. In the postabsorptive state, most of the ami- dicated by number of eggs laid and number of no acids needed for keratin synthesis are mobilized chicks hatched.89 A diet of white millet, canary from tissue proteins, although tissue (especially liv- seed, and hulled oats containing 13.4% protein er) glutathione may supply some of the required (0.32% lysine, 0.32% methionine ϩ cysteine) but cysteine. This diurnal deposition and mobilization supplemented with vitamins and minerals was in- of large amounts of tissue proteins markedly de- adequate to support reproduction. creases the ef®ciency of amino acid and energy use In growing birds, dietary protein and amino acids for molt. It also moderates the balance of dietary must be supplied for tissue accretion as well as amino acids required for molt to more closely re- maintenance. The amino acid composition of the semble the pattern in tissue protein than in feather tissues of budgerigars is very similar to that of protein.93 Molt is energetically expensive because of chickens,87 indicating that the balance of amino ac- the loss of feather insulation, the cost of synthesiz- ids required is probably similar to that determined ing feather protein, and increased body protein syn- for growing chickens. However, the higher fraction- thesis and degradation. The percentage increase in al growth rate of psittacine birds because of their the energy expenditure associated with molt often altricial mode of development might be expected to exceeds the percentage increase in protein needed increase total amino acid requirements. The require- for the molt.93 Consequently, molt may not be as- ments for growth are highest at hatch and decrease sociated with a change in the dietary amino acid over time, as the chicks' growth rate begins to slow. requirement when expressed as percentage of the The protein requirement for growth of cockatiel diet or as mg/kJ. This is because increased food chicks is 20% crude protein (CP) (1.0% methionine consumption to meet energy requirements results in ϩ cysteine, 1.5% lysine, 14.64 MJ ME/kg) for max- suf®ciently increased amino acid intake to meet re- imal growth and survivability.90 In other experi- quirements for molting. ments,91 the requirement for lysine to support max- Nutritionists must be concerned with the quality imal growth was 0.8 % of the dietary dry matter. of dietary protein sources. Protein quality varies on However, the growth rate of chicks in this experi- the basis of amino acid balance and digestibility. ment was low because of the use of a puri®ed amino For example, if 1 protein source contains a lower acid diet, and the requirement for chicks growing level of a particular amino acid compared with the at a normal rate is likely to be higher. Angel and bird's requirement (the limiting amino acid), an ap- Ballam89 found that a corn-soy based diet containing propriate complementary protein source, which is KOUTSOS ET ALÐNUTRITION OF PSITTACINE BIRDS 267

not limiting in that particular amino acid, is often favor of gradual adaptation to new dietary ingredi- used to meet the bird's requirement. Alternately, pu- ents. ri®ed amino acids can be added to the diet. The digestibility of protein by psittacine birds has not Minerals been studied in detail. Given that the assimilation ef®ciencies of complete diets are similar in psitta- Calcium is required in greater quantities than any cine birds (Table 3) and poultry, it is likely that the other mineral and is used for bone mineralization, protein digestibility is generally similar as well. metabolic homeostasis, and eggshell calci®cation. Lorikeets are an exception to this generalization. In general, the maintenance requirement for calcium Digestibility of egg white by rainbow lorikeets is is quite small. Although this requirement has not only 13.3%,86 presumably because of their small been determined in psittacine birds, the calcium re- proventriculus and gizzard. Pollen is particularly requirement for maintenance in chickens is less than sistant to digestion by lorikeets but is somewhat bet- 0.1% of the diet.94 Most seeds commonly fed to ter digested by granivorous cockatiels.57 Addition- captive birds have less than 0.1% calcium, and ally, nestlings have more ef®cient digestion than grains (eg, millet, canary seeds, corn) are especially adults. low with less than 0.03% calcium. Experimental95 Protein or amino acid de®ciency is manifested in and clinical95±97 evidence supports the contention reduced growth rates and skeletal muscle deposi- that diets based exclusively on seeds result in cal- tion.15 An amino acid imbalance may cause anorex- cium de®ciency and that the calcium requirement is ia in addition to aforementioned symptoms. De®- above 0.05%. African grey parrots are frequently ciencies of speci®c amino acids can produce dis- diagnosed with a hypocalcemia syndrome indicative tinctive pathology. For example, a methionine de- of calcium de®ciency.98 However, there is no evi- ®ciency during chick growth or molting results in dence that these species have higher than normal dark, horizontal ``stress marks'' on feathers.11 Ex- calcium requirements, and the etiology may be re- periments in which speci®c amino acid de®ciencies lated to an inability to mobilize bone stores during have been induced have not indicated increased be- acute periods of dietary inadequacy. havioral disorders such as feather picking.15 The calcium requirement for growth is expected A role of high levels of dietary protein in the to be much higher than that of maintenance on the etiology of renal dysfunction and gout of psittacine basis of the rapid rate of bone calci®cation, and re- birds has occasionally been suggested but is not quirements will likely be greatest early in life when supported by experimental evidence. Adult male the fractional growth rate is the highest. Precocial cockatiels fed 20%, 35%, or 70% crude protein for chickens require approximately 1.0% calcium, but 11 months maintained body weight and general experiments examining the calcium requirement of conditioning with no visible signs of protein tox- psittacine birds have yet to be published. In chick- icity.68 Neither uric acid precipitates nor articular ens, dietary calcium : phosphorus ratios for growth gout was observed upon postmortem examination should be maintained between approximately 1.4:1 regardless of diet. Hepatic and renal enzymes re- and 4:1, assuming that vitamin D levels are ade- sponsible for amino acid catabolism increased in quate.99 Neither the required level of phosphorus proportion to dietary protein level. However, hepat- nor its appropriate ratio to calcium is known for ic sinusoidal and periportal lipogranulomas, which psittacine birds, but clinical signs of de®ciency have might be indicative of liver damage, were found in not been widely reported despite the low levels of birds fed 70% crude protein. These data suggest that nonphytate phosphorus in seeds. levels of crude protein well above expected require- Mineralization of the eggshell requires mobili- ments are tolerated in cockatiels without clinical zation of calcium from bone; therefore, increased signs of protein toxicity, and only unrealistically levels of dietary calcium must be supplied before high levels of dietary protein result in mild liver and after reproduction to provide enough calcium pathology. Although the birds in this study were for maintenance and/or restoration of bone calcium able to adapt to high-protein diets, such adaptation density. The calcium requirement for egg produc- takes several days in chickens, and therefore grad- tion, in general, is lower for altricial than precocial ual changes were made to dietary protein levels to species, which lay proportionally larger eggs. In enable this adaptation. Sudden changes from low- chickens laying an egg a day, the calcium require- to high-protein diets might lead to hyperammone- ment is 3.3% of the diet. In contrast, in cockatiels mia, elevated uric acid or urea production, and, po- and budgerigars that lay large clutches, diets con- tentially, nephritis and gout. On this basis, it is sug- taining as little as 0.35% and 0.85% calcium, re- gested that sudden dietary changes be avoided in spectively, supported normal shell calci®cation.66,100 268 JOURNAL OF AVIAN MEDICINE AND SURGERY

The availability of calcium and phosphorus in di- tenance, without signs of de®ciency or toxicity. In ets can be extremely variable. Calcium and phos- addition, cockatiels could be maintained on a diet phorus found in plants are often less digestible than completely devoid of vitamin A (0 IU vitamin A/ other sources because of the formation of poorly kg) for 8 months, although immunocompetence was digestible complexes with phytic and oxalic acid. impaired, on the basis of reduction in secondary Calcium is usually low in grains and insects and antibody titers (E. A. K., unpublished data, Novem- high in vegetation, although bioavailability is usu- ber 2000). These data suggest that whereas the vi- ally low. In the wild, many avian species supple- tamin A requirement for maintenance is likely to be ment their diet and that of their chicks with mollusk lower than 2000 IU/kg, this dietary level is suf®- shells, eggshells, and calciferous grit.101 Some avian cient for cockatiel maintenance. In addition, devel- species, such as chickens and zebra ®nches (Peo- opment of vitamin A de®ciency in cockatiels at phila guttata) have a speci®c appetite for calcium maintenance may require prolonged periods of se- and will increase their intake of a calcium supple- verely de®cient feedstuffs. Vitamin A requirements ment (eg, oyster shell or cuttle®sh bone) when they for other psittacine species remain to be determined. are laying eggs. It is not known if psittacine birds Symptoms of vitamin A de®ciency include ke- have a similar capacity to identify and consume cal- ratinization of mucous membranes, anorexia, ruf¯ed cium-enriched foods and to match this consumption plumage, increased susceptibility to infection, and to their requirements. poor conditioning.8 In parrots, focal metaplasia of A calcium de®ciency will occur when diets con- the excretory duct or the glandular epithelium of the tain too little calcium or vitamin D (essential for salivary glands was identi®ed when liver vitamin A calcium homeostasis) or too much phosphorus. De- levels reached extremely low levels (Ͻ50 IU/g liv- ®ciency is manifested in decreased bone minerali- er).104 Liver vitamin A levels below 2 IU/g liver zation and skeletal abnormalities, particularly in were associated with extensive metaplasia of the growing birds. For example, in budgerigars, a cal- salivary glands. Symptoms of vitamin A toxicity are cium de®ciency causes a demineralization and nar- very similar, and distinguishing between de®ciency 95 rowing of the cortex of the femur. In chickens, and toxicity may require careful assessment of di- calcium toxicity is less common but results in hy- etary conditions. Interestingly, behavioral changes, percalcemia and precipitation of calcium urates speci®cally changes in vocalization patterns, were leading to kidney nephrosis. Also in chickens, signs observed when cockatiels were fed either de®cient of phosphorus de®ciency and toxicity are similar to or excessive levels of vitamin A.105 Cockatiels fed those of calcium-de®cient birds.15 100,000 IU vitamin A/kg diet had increased num- Beyond calcium, the requirement of psittacine bers of vocalizations compared with birds fed 2000 birds for other minerals is unknown. Zinc toxicity IU/kg (considered to be an adequate level for main- has been reported when very high levels (32 mg/ tenance), and the peak frequency of vocalizations day) were gavaged.102 Though these high levels was reduced. Cockatiels fed 10,000 IU vitamin A/ have never been reported in natural or commercial diets, they might be achieved if components of kg or 0 IU vitamin A/kg diet had reduced numbers poorly galvanized cages are consumed.103 of vocalizations, and 0 IU resulted in reduced peak amplitude and total power. Although vocalizations may be affected by vitamin A status, it remains to Vitamins be determined if other nutrients cause a similar Vitamin A is critical for vision, cellular differ- change. However, these data suggest that vocaliza- entiation, immune function, and numerous other pa- tion patterns may be indicative of nutrient status of rameters.8 Vitamin A, like vitamins D, E, and K, is cockatiels. a fat-soluble vitamin, and excretion of this nutrient Sources of vitamin A in the diet include plant and is much more dif®cult than for water-soluble vita- animal matter. Carotenoids from plants serve as vi- mins. On this basis, vitamin A toxicities may be tamin A precursors for chickens.106 The capacity of quite prevalent in companion bird species, and the psittacine species to convert carotenoids into vita- incidence of vitamin A de®ciency and toxicity is min A has not been studied, although on the basis reportedly quite high in captive birds.10 of foods consumed in the wild (plant based), it ap- The vitamin A requirements for psittacine birds pears that psittacine species should be quite cable are not precisely known, but recent research pro- of carotenoid conversion. In foods of animal origin, vides an indication of appropriate dietary levels. In vitamin A is abundant in the form of retinyl esters, adult female cockatiels, diets containing 2000 or which are considered to be highly available.6 10,000 IU vitamin A/kg were suf®cient for main- Both vitamin A and D toxicosis have been re- KOUTSOS ET ALÐNUTRITION OF PSITTACINE BIRDS 269 ported in macaws as a result of misuse of liquid laying kakapo hens select a diet that apparently is vitamin supplementation.107,108 de®cient in essential fatty acids even when foods that can meet the requirement are available.110 Other nutrients The nutritional characteristics of food items from domestic plants are often very different from those Psittaciformes, like other avian species, require from native plants. In general, seeds from domestic essential fatty acids, and numerous vitamins and plants are more concentrated in energy and lower trace minerals in addition to those described above. in protein and many other essential nutrients than Unfortunately, research concerning requirements for seeds available in the wild.15 Likewise, domestic these nutrients is lacking. Therefore, assumptions fruits and vegetables are higher in energy and water must be made based upon poultry literature and but lower in other essential nutrients compared with knowledge of Psittaciforme physiology when for- relatives in the wild.111 These food items can form mulating Psittaciforme diets. the basis of diets for humans when part of a varied The degree to which dietary carotenoids are diet, but humans grow very slowly and have a very needed for pigmentation of feathers of Psittacifor- low reproductive output relative to any avian spe- mes is not well characterized. Efforts to identify cies. Young psittacine chicks double their body carotenoids of dietary origin in the feathers have not weight in a few daysÐa feat that requires more than been successful109 and cockatiels can be maintained a year in humans. Poultry are more similar, though for over a year on carotenoid-free diets with no loss still slower, to psittacine birds in growth rates. Do- of feather coloration (E. A. K., unpublished data, mestic seeds are used as the basis of poultry diets, August 2000). Furthermore, chicks hatched from but they must be heavily forti®ed with amino acids, these birds develop normal yellow and orange vitamins, and minerals to provide nutritionally com- feather colors even when fed carotenoid-free diets. plete diets.6 Both controlled experiments5 and clinical experiences3,14,112 clearly show that domestic Captive Diets seeds must also be supplemented when used as the The diets consumed by free-living birds can rare- basis for diets of psittacine birds. Ullrey et al5 com- ly be duplicated in captivity because the vast range pared the nutritional content of seeds commonly of seeds and other food items are not usually avail- used in commercial avian diets with estimated re- able in suf®cient quantities. Even if these food quirements of psittacine birds and concluded that items, or very similar ones, could be obtained, they they were typically de®cient in amino acids, calci- may still not be nutritionally adequate. This is be- um, available phosphorus, sodium, manganese, cause birds usually eat a quantity of food necessary zinc, iron, vitamins A, D, K, and B-12, ribo¯avin, to satisfy their energy needs, and free-living birds pantothenic acid, choline, and available niacin. Io- have to expend considerable energy to support ther- dine and selenium may be de®cient, depending moregulation, extensive foraging, defenses, etc (see upon the geographical region of production. Nutrient Requirements: Energy). Thus, the amount Attempts have been made to correct the nutri- of food consumed by a free-living bird is much tional balance of domestic seeds by coating them greater than the amount of the same foods con- with vitamin and mineral solutions or providing sumed by that bird in captivity. However, the daily supplement pellets in with the seeds. However, seed need for amino acids, minerals, and vitamins is rel- coatings are mostly lost when the bird removes the atively constant regardless of energy expenditure. husk, and supplemented pellets are not often con- Therefore, birds in captivity must acquire the same sumed. For example, when African grey parrots daily quantity of essential nutrients as free-living were presented with a mix of seeds (sun¯ower, pea- birds but with much less food consumed. Conse- nuts, saf¯ower), oranges, a variety of vegetables, quently, the concentrations (g/kg) of amino acids, and a nutritionally complete supplement, they se- vitamins, and minerals must be higher in captive lected a mostly seed diet and consumed only 11% diets than wild diets, and food items that might be of the dry matter from the supplement.5 This self- suf®cient for a wild bird can be inadequate for the selected diet was de®cient in 12 vitamins, minerals, same bird in captivity. Additionally, birds in the and amino acids. wild do not always have the nutritional wisdom to Forti®cation of nutrients through the water is select adequate diets. Many animals are able to bal- problematic for 2 reasons. First, an aqueous solution ance energy, amino acid, and calcium levels in their of vitamins and minerals is very unstable, and many diets by selecting among dietary items, but there is vitamins are destroyed because of the high redox little evidence that animals can select for adequate potential of minerals, especially iron, zinc, and cop- levels of many other nutrients. For example, egg per. Second, as described above, rates of water con- 270 JOURNAL OF AVIAN MEDICINE AND SURGERY sumption are extremely variable among individuals Table 6. Fledging percentage in 8 birds in the order within a species and seasonally, resulting in situa- Psittaciformes fed diets based on seeds versus diets tions of nutrient de®ciencies or excesses. based on nutritionally complete extruded pellets.a Another dietary approach is to provide pelleted or extruded mixtures of ingredients that provide all Species Seeds Extrusionb of the required nutrients at levels above the esti- Yellow-headed Amazon 75 100 mated requirements. The processing adheres all of (Amazona ochrocephal ortrix) the dietary ingredients together so that the bird can- Forsten's lorikeet 62 100 not select individual components that would result (Trichoglossus haematodus forsteni) in a nutrient imbalance. This approach has been Goldie's lorikeet 45 83 used very successfully for domestic animals, in- (Trichoglossus goldiei) Blue and gold macaw 62 80 cluding poultry, for many decades. It has more re- (Ara ararauna) cently been applied with success to a variety of psit- Scarlet macaw 62 100 5,13,112 tacine species. (Ara macao) Complete diets are usually based on ground Ring-necked parakeet 80 100 grains, such as corn, to supply energy and ground (Psittacula krameri manillensis) legumes, such as soybean meal or peanut meal, to Rock peplar parakeet 88 80 supply protein. Vitamins, minerals, vegetable oil, (Polytelis anthopeplus) and puri®ed amino acids are added in appropriate Blue-crowned hanging parakeet 50 75 amounts to make up for de®ciencies in the grain (Loriculus galgulus) and protein sources. In practice, 2 primary criti- Mean 66 90 cisms of pelleted diets have been voiced: reluctance a From Ullrey et al.5 of seed-adapted birds to switch to pellets and con- b Parents were provided with a mixture of seeds (corn, sun- cern over the lack of variety and enrichment offered ¯ower, peanuts, saf¯ower) or nutritionally complete extruded pellets. Oranges and vegetables were also provided to both 112 by pelleted diets. An array of protocols to facili- groups. tate conversion has been published in the popular literature. Once birds have been converted to a pelleted diet, the preference of their offspring for seeds body weight. Requirements increase for the female is greatly diminished. Dietary enrichment can be a few days prior to egg production and remain el- accomplished by providing the majority of the nu- evated until the clutch is laid.15 Two different diets trition via pellets but also supplying an assortment are often utilized to accommodate these changing of fresh fruits and vegetables.113 Pelleted diets can needs: a grower-breeder diet and a maintenance be formulated so that they complement fruits and diet. A grower-breeder diet that meets the require- vegetables that are offered as part of the diet. This ments for a growing chick would also likely meet is accomplished by increasing the nonenergy com- the requirements of the hen for egg production. ponents of the pellets so that the nutrient dilution Consequently, this diet can be introduced at the time due to consumption of fruits and vegetables is cor- birds begin to show nesting behavior and continue rected. Domestic vegetables and especially fruits are to be fed until chicks have ¯edged. The need for a predominantly water, so relatively large amounts special diet for periods of molting has yet to be can be provided without seriously compromising established. the overall quality of the diet. Ullrey et al5 dem- Parents feed their chicks a mixture of food and onstrated the ef®cacy of providing an extruded water. They are apparently very adept at providing complete diet together with fruits and vegetables for the appropriate proportions of food and water and 8 different species of breeding psittacine birds (Ta- delivering it in the correct amounts and frequencies. ble 6). In this study, the ¯edging success was con- At least in crimson rosellas (Platycercus elegans), siderably greater when the pelleted diet was fed in parents are able to discriminate individual chicks place of seeds (90% versus 66%, respectively). and provision them at different rates depending upon their hatching order.114 In many circumstances, Diets for the Life Cycle hand-feeding of hatchlings is desirable or essential. Special formulated diets based on more water dis- The nutrient requirements and the optimal diet persible ingredients facilitate hand feeding. These for an animal change throughout the life cycle. Re- diets are mixed with appropriate amounts of water quirements (g/kg diet) are usually highest in the and delivered to the back of the chick's mouth. hatchling when growth is rapid and decrease until Roudybush and Grau90 conducted a series of exper- they reach a minimum after the bird reaches adult iments to determine the appropriate ratio of feed to KOUTSOS ET ALÐNUTRITION OF PSITTACINE BIRDS 271 water to provide during the growth periods. The ra- syndromes. In: Rosskopf WJ, Woerpel RW, eds. Dis- tio that maximized survivability depended upon the eases of Cage and Aviary Birds. Baltimore, MD: Wil- age of the chicks. For the ®rst 4 days after hatch, liams and Wilkins; 1996:260±282. 7% solids and 93% water was optimum, but there- 4. Robben JH, Lumeij JT. Comparative studies on parrot after 30% solids were needed. Insuf®cient water foods commercially available in The Netherlands. Tijdschr Diergeneeskd. 1989;114:19±25. during the ®rst few days after hatch results in high 5. Ullrey DE, Allen ME, Baer DJ. Formulated diets ver- mortality, whereas insuf®cient solids later on results sus seed mixtures for psittacines. J Nutr. 1991;121: in slow growth rates. Growth rates of hand-fed S193±S205. cockatiels lag somewhat behind those fed by their 6. NRC. Nutrient Requirements of Poultry. Washington, parents. Presumably this is because parents feed DC: National Academy Press; 1994. their chicks throughout the night and provide meals 7. Brue RN. Nutrition. In: Ritchie BW, Harrison GJ, Har- more frequently than typical hand-feeding sched- rison LR, eds. Avian Medicine: Principles and Appli- ules. However, parental provision of nutrients, com- cation. Lake Worth, FL: Wingers; 1994:63±95. mensal micro¯ora, or possibly even protective mol- 8. Lowenstine LJ. Nutritional disorders of birds. In: ecules cannot be ruled out. Fowler ME, ed. Zoo and Wild Animal Medicine. Phil- adelphia, PA: WB Saunders; 1986:201±212. 9. Harrison GJ, Harrison LR. Nutritional diseases. 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