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Nutrition in Psittaciformes: scientific background and practical application Bachelor thesis Veterinary Medicine, Utrecht University Supervisor: dr. J.T. Lumeij Author: Natasja Slooten Student number: 0148628 Date: 17-04-2012

Summary In the nutrition of psittacine birds, different types of feeds with different nutritional values exist. This review integrates information of the nutritional requirements of psittacine birds and nutritional values of seed mixtures and extruded pellets. The nutritional value of seed mixtures is extremely low compared to that of extruded pellets. It is seen that when the dehulled seeds are analyzed the energy and protein content related to the volume meets the energy requirement and protein needs of psittacine birds. Still the dehulled seeds show low contents of calcium and vitamins. Extruded pellets meet the nutrient requirements of psittaciformes in most ways. Human food can have low contents of energy, protein or minerals related to the volume. This means, when given next to a seed mixture or extruded pellets, it can lower the energy, protein and mineral content of the nutritional intake. This is, because parrots in captivity eat limited by volume. When a parrot owner gets the recommendation of a pet shop employee to buy a seed mixture, it explains why the parrot owner does not know enough about the nutritional requirement of their parrot. Fifty percent of the pet shops have the appropriate knowledge of nutritional requirement of psittacine birds, but the products like extruded pellets are in half of the tested pet shops absent. Confronted with this situation it is extremely difficult for the parrot owner to buy the right food based on the right knowledge. Introduction In veterinary practice owners are seen who don’t have any idea what the nutritional requirement is of their psittacine birds. They believe that the daily refreshment of the seeds these parrots are given is enough for a long healthy life. A psittacine bird does not eat each seed of the offered seed mixture, but eats selective. This is the most common reason a psittacine bird can develop malnutrition. Rickets, osteomalacy, atherosclerosis, keratinization of the tissue and difficulty in laying eggs are examples that are observed. Cases of real malnutrition are seen less in veterinary practices than 10

years ago. Still there is a long way to go before (potentially) owners of parrots have adequate knowledge to feed their parrot appropriately. A kind of standard already exists for a complete nutrition for dogs and cats, so their owners know very well what their animals need. Almost all owners of psittacine birds want the best for their pets. So why don’t they know enough about the nutritional requirement of their psittacine bird? And where is the transfer of information blocked, so that (potentially) owners of parrots are not well informed about a complete nutrition? This is concerning. If they are well informed, they can give their psittacine birds extruded 1

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pellets. These extruded pellets exist in all different kinds. In relation to these pellets this review will evaluate in more concrete terms the following questions. What is the nutritional value of seed mixtures in relation to that of pellets? What is the difference between the pellet brands and is there any difference between these brands that can result in malnutrition? This article will answer these questions by reviewing information that is available about this subject. Because pet shops play a central role in information about this subject, a market research to the kind of information they give about nutrition of psittacine birds is done. Digestive anatomy of psittacine birds The digestive anatomy of psittacine birds differs extremely from the mammalian digestive tract. It consists with the beak, a toothless mouth, tongue, pharynx, esophagus, crop, proventriculus, gizzard, intestine, rectum, cloaca and vent. The digestive anatomy among different species of birds is extremely variable. Species of birds with similar feed preferences often have similar digestive tracts. Species consuming nectar and fruits, which are easy digestible, have short and simple digestive tracts. Species consuming seeds and animal matter, which need more enzymes to digest, have large stomachs and small lower intestines. Species consuming plant cell walls, which are very difficult to digest, have large ceca for fermentation. This is relative to body size. (Klasing, 1998) In many species of birds, parrots included, the crop plays an important role in feeding the young by regurgitating the stored food. The stomach is divided in two parts, the proventriculus (the glandular part) and the gizzard (the muscular part). The proventriculus secretes enzymes, hydrochloric acid and pepsin, and is very

large in many carnivores and piscivores. The gizzard is on the other hand very muscular and bigger than the proventriculus in granivores and herbivores. In parrots the gizzard is less muscular, because they dehull the seeds before swallowing. Because nectarivores and frungivores have an easy digestible diet, their gizzard is only a small diverticulum. In this small diverticulum occasionally consumed insects will be digested. The size of the gizzard may adapt to the consumed diet by changing the volume. This means that in many birds the gizzard size has a seasonal fluctuation, because the diet changes during seasons. The small intestine is less variable, but the length and the type of villi changes between species. Herbivores and granivores have a long small intestine. However carnivores, nectarivores and frungivores have a short small intestine. Meat or fruit is quickly digested compared to digestion of seeds or plant cell walls. (Duke, 1997) Many birds have ceca and different types of ceca are known, but ceca are absent in psittacine birds. This means that psittacine birds lack the function of ceca. This function is microbial fermentation, extra water absorption, nitrogen excretion and may serve as a secondary lymphoid tissue. Nutritional requirement of wild psittacine birds Wild birds in general have evolved in a specific habitat in which their nutritional requirement is fulfilled. Birds in captivity eat what is given by the owner. This may explain obesitas in psittacine birds in captivity. (Ritchie et al., 1994) Also a low energy or nutrient intake can be explained when a psittacine bird eat an amount of food which contain too low energy or nutrients. The natural diet of wild psittacine birds consists of a wide variety of ingredients which include indeed seeds and nuts, but 2

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also other parts of plants, such as flowers, buds, leaves, fruit and bark, insects and larvae and meat of carcasses. (Ullrey et al., 1991) The nutritional requirement of psittacine birds can be derived from the nutritional requirements of poultry and game birds, from food habits of wild birds and from information on trial and error feeding. (Nott et al., 1994; Donoghue et al., 1997; Koutsos et al., 2001) Food habits of wild birds are not well known, so this article will discuss the nutritional requirement of psittacine birds by analogy of poultry and from information on trial and error feeding. Nutritional requirement of companion psittacine birds Different methods are used to approach the requirement of a specific nutrient in a bird. The easiest one is to examine the nutrient’s influence on growth. In experiments birds are fed with a specific diet with a certain quantity of a nutrient. At the point that there is no further increase in growth, this would be considered to be the growth requirement of that specific nutrient. This is now the suggested highest level of this nutrient. Studies about specific nutrient requirements for pet birds are rare, because the determination of nutrient requirement is extremely difficult. That is why nutrient recommendations, after extrapolation from poultry species, are used for companion pet birds. (Brue, 1994) The recommendations that were made in Brue’s study are in percentage (%). However, to compare the different seed mixtures and pellets, we will use the nutrient needs on energy basis (g/MJ). The nutrient requirement for maintenance is the lowest level of this nutrient and is needed to maintain metabolic functions and

body temperature. All nutrient levels are minimized, because the primary need is for replacement and lost. Of course growth, breeding, sickness, stress and moulting may need more nutrients than strict maintenance. Breeding costs more protein and calcium, so is needed in the diet. Also stress responses in the bird’s body to mobilize and produce glucose for the increased energy need. (Ritchie et al., 1994) Energy requirement The energy content of the feed is not the same as the metabolizable energy the parrot finally uses for his body’s metabolic processes. After losing energy sources through the feces, urine, gasses and urates the metabolizable energy (ME) remains. (Harper, 2000) Psittaciformes make energy from carbohydrates, fat and protein in the diet. Protein is the least efficient energy source, because the bird’s body works hard to break down the proteins to amino acids and to excrete the formed nitrogen. When veterinarians have to tube-feed a bird, when the bird itself does not eat or needs extra energy by causes as surgery, trauma and sepsis, they calculate the BMR (= requirement for complete inactivity) of the bird. In this equation (formed by Sedgwick et al.) BMR (kcal/day) = K (W kg 0.75) K is a theoretical constant for kcal used during 24 hours for various species of birds, mammals and reptiles. K = 78 for nonpasserine birds. (Sedgwick et al., 1990) The maintenance energy requirement (MER) is the BMR plus the energy needed for digestion, absorption and normal physical activity. The MER can be 1.3 to 7.2 times the BMR and depends on the energy needed 3

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for activity and thermoregulation. For psittaciformes in captivity with normal activity we use a MER 1.5 times the BMR to calculate the daily energy requirement. (Ritchie et al., 1994) If we want to calculate the MER by this method of an African Grey parrot with a weight of 400 grams, this bird needs 58.8 kcal/day. According to Harper this equation underestimates the maintenance energy expenditure requirements of all the species of birds. (Harper, 2000) This underestimation is due to the fact that the energy requirement of maintenance is correlated to the body mass and the relative size of the different organs, because these are the tissues that use oxygen. (Daan et al., 1990)

maintenance energy expenditure and is derived of the ME (metabolizable energy) by adding 25%. This 25% is the additional energy costs of uric acid formation and food assimilation. W is the weight in grams. (Harper et al., 1998)

However, energy requirement based on metabolic body weight forgets another important factor in energy requirements. This is the body composition. The metabolic rate of fat is much lower than that of muscle and liver. (Scott et al., 1992) This means that the lean:fat ratio in the body has influence on the energy requirement. Freeflying birds that are physically active have a high lean:fat ratio and thus a high BMR and MER. Captive parrots in cages, like most pet parrots, have a low activity and may have a lower lean:fat ratio. This results in a lower BMR and MER.

Calcium needs

The study of Harper shows that an equation derived for a particular body weight is more useful than a general equation derived for a wide range of body weights. This study derived the energy requirement for pet birds by studying their daily energy expenditure. Two suitable equations for calculating the energy requirements of pet birds were those derived over ranges of body weight. MEE (kcal/day) = 0.62 W gr 1.1 This is the equation for pet birds with a weight less than 100 gram. MEE is the

MEE (kcal/day) = 4.55 W gr 0.55 This is the equation for pet birds between 100 and 1500 grams. (Harper et al., 2000) If we use this equation to calculate the energy requirement for the example of the African Grey parrot with a weight of 400 grams this bird needs 123 kcal/day. This is almost three times more metabolizable energy requirement than in the equation of Sedgwick et al.

Calcium is an essential mineral needed for the skeleton, but it also plays an important role in the body fluids to activate enzyme systems and maintains excitability of the muscles and heart. Calcium is absorbed in the small intestine with the help of a calcium-binding protein. Decrease of calcium absorption occurs when compounds as phosphates, oxalates and phytate form complexes with the calcium. The same happens when high amount of free fatty acids are present in the intestines. (Ritchie et al., 1994) Avian calcium metabolism is mainly characterized by the ability to lay large eggs with a calcified eggshell. A female bird increases the intestinal absorption and resorption of calcium of the medullary bone to require the calcium for eggshell calcification. (Klasing, 1998) A shortage of calcium is the most observed mineral deficiency in birds. Rickets, osteomalacy and difficulty in laying eggs are observed. An extremely high calcium intake may lead to toxicity. This is why a maximal level of calcium intake exists. Also the ratio 4

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of calcium to phosphorus is important, because the availability of calcium for intake can decrease when the ratio is less than 1. (de Matos, 2008) Different researches suggest different optimum calcium levels. For instance Mc Donald suggests optimum calcium levels between 0.3 % and 0.7 %. (Mc Donald, 2006) This means a minimum of 0.24 g/MJ and a maximum of 0.56 g/MJ. On the other hand the study of Schoemaker recommends optimum calcium levels between 0.2 g/MJ and 1.0 g/MJ. (Randall, 1981) Vitamin needs Vitamin A needs Vitamin A is needed for vision, but more important in birds is its effect on the epithelial tissues, its growth and differentiation. A shortage of vitamin A in birds results in keratinization of mucous membranes, poor conditions and increased susceptibility to infection. Plants do not contain active vitamin A, but contain precursors of vitamin A. These are carotenoid plant pigment, with the carotenes being the most important. Intoxication does not occur so quickly, unless an excess of 1000 times of the requirement is given. A minimum need of vitamin A is 645 IE/MJ. (Schoemaker et al., 1999) The levels are adapted from the Exotic Bird Nutrition Expert Panel Report, Nutrition and Management Committee of the Association of Avian Veterinarians in 1996. Vitamin D3 needs No research is done to find optimum and toxic levels of Vitamin D3 in the diet for pet psittacine birds. Schoemaker recommends optimum levels of Vitamin D3 with a minimum of 40 IE/MJ and a maximum of 161 IE/MJ. (Schoemaker et al., 1999)

Protein needs In a study with growing cockatiels, these birds were fed with different percentages of crude protein in the diet. Those fed a 20% crude protein diet, reached the weaning stage earliest. Those fed a 10% or 15% crude protein diet grew slower. Those fed a higher than 20% crude protein diet developed behavior problems (like meal refusal) and growth depression. (Grau et al., 1985) These are results from growing parrots and of course the level of crude protein needed by growing parrot is higher than needed by an adult parrot for maintenance. Westfahl quantifies the inevitable N losses via excrements. Eight adult Amazons were fed with an N-free diet. The results showed a minimum protein need of 1.9 g/kg BW0.75/day and this means 4-5 % required protein content. N losses via feathers and skin cells are excluded in this value. Including the N losses via feathers and skin cells, when compared with results in budgerigars of other publications, this leads to approximately 6-7% required protein content. This means a protein requirement of 4.83-5.64 g/MJ protein. (Westfahl et al., 2008) The outcome of this study is less than needed by budgerigars (9-10%, 7.25-8.06 g/MJ) (Drepper et al., 1988) and cockatiels (11%, 8.87 g/MJ) (Koutsos et al., 2001). This is a much lower percentage than Schoemaker proposes. He proposes a minimum of 12 % (9.7 g/MJ) of crude protein intake as an optimum diet. (Roudybush et al., 1991) Fat needs Fat is an important energy source and is the primary storage form of energy in the body. Fat itself is not required, but the bird’s body cannot make certain fatty acids itself. These are so called essential fatty acids and must 5

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be present in the diet. The primary essential fatty acid is linoleic acid. The uptake of linoleic acid has probable a negative influence on the existence of atherosclerosis. (Bavelaar et al., 2003) Based on the requirements of most other species, the linoleic acid requirement for parrots can be safely derived as more than 0.8 g/MJ. (Ritchie et al., 1994) Carbohydrate needs Carbohydrates, like glucose, are the most important energy source, because this is the only energy source the brain can use. Energy is derived from monosaccharides, disaccharides and starches. The fiber fraction of the diet is also formed by carbohydrates, but these are undigestible carbohydrates. The cellulose in this fiber fraction cannot be digested because of the lack of the enzyme cellulase in birds. This is why the carbohydrate requirement of psittaciformes is not examined, because at the same time glucose is used by all cells in the body and fibers are useless. (Ritchie et al., 1994) Nutritional value of seed mixtures and extruded pellets The nutrient analysis of commercial seed mixtures differs from the nutritional intake, because parrots dehull most seeds. Besides most seed mixtures lack information concerning their nutrient analysis, because in most European countries it is not obliged to supply the analysis. (Werquin 2005) A study of Werquin compared the nutrient composition of the total seed mixtures with that of the kernels. The nutrient composition of the kernels was compared with the commercial pellets. A big difference is the higher mean fat and energy content in kernels compared with the total seed mixtures. Fat and energy contents of the

commercial pellets were extremely lower compared with the kernels. Werquin assumed that the fat (8.6 4.1 %) and energy (15.6 14 MJ ME/kg) content of the commercial pellets might be too low for optimal feeding. (Werquin et al., 2005) The pellets for parrots which are reviewed in this article are produced under low heat extrusion and differ from the real term pellets. Pelleting uses steam, pressure and a binding agent to bind the grains into a firm pellet. Extrusion has the same steps involved with baking, which is mixing, kneading, proofing, shaping, rising and cutting. The carbohydrates expand when heated, in addition to the heat effects, and put under pressure and the pressure released. It is comparable with popcorn, where the grain is exploded into a white fluffy ball that maintains its shape and fluffiness upon cooling. (Hand et al., 2000) The protein contents in commercial pellets were all higher than 7.5 g/MJ ME and thus seemed to be appropriate (Kamphues et al., 1997). Bavelaar did a nutrient analysis of commercial seed mixtures and pellets. These analyzed seeds were not dehulled. Bavelaar found that commercial pellets have a higher protein content than seed mixtures, which were not dehulled. Three of the seven brands of pellets; Bingo (NASCK Veterinary Products Inc), Adult Life Time (Harrison’s Bird Diets) and Happy brok (Fitas Trading B.V.) have a low protein content. Even one pellet brand (Avi-products Parrot Bix) has a calcium content too high, this could lead to toxicity. The recommended pellet brands which meet the nutritional requirement of parrots in most ways are Exact Rainbow (Kaytee Prosucts Inc), High Potency (Harrison’s Bird Diet) and Nutribird P15 (Versele-Laga). Nutribird P15 (VerseleLaga) has also the highest content of linoleic acid. (Bavelaar et al., 2003) 6


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All seed mixtures in the study of Werquin had a very low calcium content. There was no difference between the seed mixtures and their dehulled fractions. On the other hand, the phosphorus levels in the dehulled seed mixtures were significantly higher than in the seed mixtures. This has a negative influence on the calcium/phosphorus balance. The commercial pellets had higher calcium levels and better calcium/phosphorus balance. The sodium content of the seed mixtures were too low, but appropriate in commercial pellets. This research shows that the analysis of the not dehulled seed mixture underestimates the energy content of their ingested portions with 36%. The nutrient analysis of the dehulled fraction of the seed mixture gives us an idea of the real parrot diet. Birdfood producers should be encouraged to provide these data. The specific feeding behavior of parrots, being selective eaters and dehulling/dehusking of seeds, changes the nutritional intake compared with the nutritional value of seeds diets. Seed kernels contain a higher amount of phosphorus but a lower amount of calcium in relation to whole seeds. This worsens the already

suboptimal Ca:P ratio. (Werquin et al., 2005) Eating of excess fruit and vegetables lowers the energy density of a diet (Donoghue et al., 1997). A feeding trial done by Kalmar on six yellow-shouldered amazons assessed the nutritional impact of parrot-specific feeding behavior and the influence of additional provision of fruit next to the seed mixture. Provision of fruit in combination with seed diet lowered voluntary energy intake, without an adequate protein intake. This can be applied in case of obesity. (Kalmar et al., 2010) In the study of Hess 135 pet birds were examined to determine their weekly food consumption. Two independent laboratories analyzed the formulated products and seeds for their nutrient content. The outcome of this study showed that pet birds consuming less than 50 % of their diet from pellets had insufficient intakes of vitamin A and D3 and calcium. Diets with a high percentage of human food were low in protein, energy, vitamins and minerals. Diets with a high percentage of seeds were high in fat and deficient in vitamin A and D3 and calcium. (Hess et al., 2002)

Table 1: Summary of nutrient analysis for different types of food for psittaciformes Nutrient analysis

Seed mixtures

Energy Calcium Vitamin A Vitamin D3 Protein Linoleic acid

Low Low Low Low Low High

Dehulled seed/kernels High Low Low Low High High

Information to the public No obligatory education requirements exist for employees who work in a pet shop. In

Extruded pellets

Human food

High High High High High High

Low High Low Low Low High

the future the DIBEVO (Dutch organization of pet shop retailers) wants to introduce a kind of professional degree for employees of a pet shop. Right now anyone can open a pet 7

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shop and work there. There is no specific knowledge needed to sell bird food or even sell a bird. (Source: DIBEVO) Most seed mixtures lack information concerning their nutrient analysis, because in the Netherlands it is not obliged to supply the analysis. This nutrient analysis on the packing of animal food is only obliged by law for dogs, cats and fur-bearing animals. When there is a nutrient analysis on the packing of food for psittaciformes the VWA (Dutch Food Authority) can ask for an explanation. The only thing what is obliged by law is that on the packing of the animal food there has to be an instruction how to use it by the owner. This means how much of the food is needed per day and that it has to be supplied in combination with water. A warning for selective eating of these psittaciformes is not obliged. In this way a random person with no knowledge of parrots can develop a seed mixture for parrots and sell it on the market. The only thing what this person has to do is to register as a food company for animals. (source: produktschap Diervoeding) This may be a reason why so many pet shop owners and breeders recommend their own brand of seed mixtures as the best for a parrot. LICG is a dutch institute that claims to give objective and independent information about buying and taking care of pets responsibly. Their main ambition is to improve the health of pets. The information they give about buying and taking care of pet birds is extremely wide, which may be too overwhelming for (potentially) parrot owners. For seventeen different species of birds they developed a so called leaflet with information about the pet bird’s natural habitat, accommodation, nursing, nutritional requirement, reproduction, diseases and acquisition costs. They did not focus on the main problem in veterinary medicine of

birds, which is malnutrition. They advice to feed a psittacine bird a mixture of extruded pellets, fruits, vegetables and a little amount of seeds as nuts to give as rewards. This advice leads a lot of room for the owner to create their own ideal meal for their pet bird, which leads most of the time to a pet bird which eats more or only seeds instead of the other offered extruded pellets, fruits and vegetables. In the same advice of the LICG owners are recommended to buy their extruded pellets in pet shops and veterinary clinics. In the little market research which is done, half of those shops do not have any extruded pellets in assortment. This makes it extremely hard for the parrot owner to get the right food for their pet bird. (source: LICG) In the explorative market research it is concluded that the knowledge of pet shop employees differs extremely. In this little research ten different pet shop employees in Amsterdam en Utrecht were asked for the best nutrition to feed a parrot. Fifty percent of the investigated pet shop employees tell about the existence of pellets when asked about the best feeding for parrots. The remarkable fact is that these same shops do not sell these recommended pellets, but only the seed mixtures. Other pet shop employees recommend their own brand of seed mixtures, while in those cases the extruded pellets were available in the shop. Only one pet shop could tell exactly the benefits of the extruded pellets, but also how difficult it is to change the feed behavior when a parrot is used to eat seeds. With a lot of information about slowly changing the diet this pet shop was a favorable exception. It is possible that pet shops are afraid of unhappy customers when selling the extruded pellets, because of these difficulties in changing feed behavior.


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Conclusion The nutritional value of seed mixtures is extremely low compared to that of extruded pellets. It is seen that when the dehulled seeds are analyzed the energy and protein content meets the energy requirement and protein needs of psittaciformes. Still the dehulled seeds show low contents of calcium and vitamins. Extruded pellets meet the nutrient requirements of psittaciformes in most ways. Human food can have low contents of energy, protein or minerals related to the volume. This means, when given next to a seed diet or pellet diet, it can lower the energy, protein and mineral content of the nutritional intake. This is, because parrots in captivity eat limited by volume. When a parrot owner gets the recommendation of a pet shop employee to buy a seed mixture, it explains why the parrot owner does not know enough about the nutritional requirement of their parrot. Fifty percent of the pet shops have the appropriate knowledge of nutritional requirement of psittacine birds, but the products like extruded pellets are in half of the tested pet shops absent. Confronted with this situation it is extremely difficult for the parrot owner to buy the right food based on the right knowledge. Discussion In many studies the authors assume that psittaciformes eat to meet their energy requirements and can control their energy intake very carefully. They base this on a study from 1954, a study of the energy requirement of chickens. (Hill et al., 1954) They automatically make a comparison to parrots. But parrots in captivity are not the same as parrots in the wild.

Bavelaar et al. came to the conclusion that three of the seven analyzed pellets had a too low protein content. They used a protein need for parrots which has to be more than 9.7 g/MJ. This recommended protein need is adapted from the protein need of poultry. Westfahl however, after a research to the protein needs of amazons, concluded to a much lower need of protein, namely 4.83-5.64 g/MJ. Considering that the study of Westfahl is much more accurate we can conclude that the protein content of all the pellets is sufficient.

This shows very clearly that more research is needed among psittaciformes to determine the nutrient needs in a more exact way. Research results from the field of poultry should be regarded with reluctance. In the study of Hess human food was one category and this was not specified. This means that they did not make any difference between French fries with mayonnaise for example and a salad. The fries contain a lot of energy in contrary to the salad. It is very urgent that the producers of certain seed mixtures should be obliged to do a nutrient analyse and show it clearly on the package. This should apply not only for the seed mixture, but also for the dehulled fraction. Also a warning should be added on the package, that when the parrot eats selectively, the product (in this case the seed mixture) is not well used and may cause malnutrition. References National Research Council Nutrient Requirements of Poultry. 8th rev ed. Washington, DC: National Academy Press; 1982. Bavelaar F.J., Beoordeling

Beynen van

A.C. (2003). commerciele 9

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papegaaienvoeders. Tijdschrift Diergeneeskunde 23, 726-734


Nutrition. Missouri: Walsworth Publishing Company, 127-146

Bavelaar F.J., Beynen A.C. (2003) Severity of artherosclerosis in parrots in relation to fatty acid composition of breast muscle or adipose tissue as biomarkers of fatty acid intake. Avian diseases 47, 222-233

Harper E.J., Lambert L., Moodie N. (1998) The comparative nutrition of two passerine species: the canary (Serinus canarius) and the zebra finch (Poephila guttata). J Nutr. 128, 2684

Brue R. (1994). Nutrition. In: B.W. Ritchie, G.H. Harrison, L.R. Harrison (eds), Avian Medicine: Principles and Application, Wingers Publishing, Lake Worth, 71.

Harper E.J., Clark C., MacDonald D.W. (2000) Energy metabolizability and nutrient digestibility in the blackgilled magpie pica pica. Ibis 143, 216-221

Daan S., Masman D., Groenewold A. (1990) Avian basal metabolic rates: their association with body composition and energy expenditure in nature. Am J Physiol. 259, 333–340

Harper E.J. (2000) Estimating the energy needs of pet birds. Journal of Avian Medicine and Surgery 14, 95-102

De Matos R. (1998) Calcium metabolism in birds. Veterinary Clinics Exotic animal Practice 11, 59-82 Donoghue S., Stahl S. (1997) Clinical nutrition of companion birds. Journal of Avian Medicine and Surgery 11, 228-246 Drepper K., Menke K. H., Schulze G., Wachter-Vormann U. (1988) Untersuchungen zum Protein und Energiebedarf adulter Wellensittiche (Melopsittacus undulatus) in Kafighaltung. Kleintierpraxis 33, 57–62. Duke G.E. (1997) Gastrointestinal physiology and nutrition in wild birds. Proceedings of the Nutrition Society 56, 1049-1056 Grau C.R., Roudybush T.E. (1985) Protein requirement of growing cockatiels. Proc 34th West Poult Dis Conf, 107-108 Hand M.S., Thatcher C.D., Remillard R.L., Roudebush P. (2000) Small Animal Clinical

Hess L, Mauldin G., Rosenthal K. (2002) Estimated nutrient content of diets commonly fed to pet birds. The veterinary record 150, 399-404 Hill F.W., Dansky L.M. (1954) Studies of the energy requirements of chickens. 1. The effect of dietary energy level on growth and feed consumption. Poult Sci. 33, 112–119 Homan H.J., Stahl R.S., Linz G.M. (2011) Comparing a bioenergetics model with feeding rates of caged European starlings. Journal of wildlife management 75, 126-131 [let op: betreft Passerines] Kalmar I.D., Werquin G., Janssens G.P.J. (2007) Apparent nutrient digestibility and excreta quality in African grey parrots fed two pelleted diets based on coarsely or finely ground ingredients. Journal of animal physiology and animal nutrition 91, 210-216 Kalmar I.D., Veys A.C., Geeroms B., Reinschmidt M., Waugh D., Werquin G., Janssens G.P.J. (2010) Effects of segregation and impact of specific feeding behavior and additional fruit on voluntary 10

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nutrient and energy intake in yellowshouldered amazons (Amazona barbadensis) when fed a multi-component seed diet ad libitum. Journal of Animal Physiology and Animal Nutrition 94, 383-392 Kamphues J., Wolf P., Bayer G., Wentker M. (1997) Basic data on the composition of seeds and feeds used in pet bird nutrition. Ubers. Tierernahrg. 25, 205 Klasing K.C. (1998) Comparative avian nutrition. Cab International. New York. Koutsos E.A., Smith J., Woods L., Klasing K.C. (2001) Adult cockatiels (Nymphicus hollandicus) undergo metabolic adaptation to high protein diets. Journal of Nutrition 137, 2014-2020 McDonald D. (2006) Nutrition and dietary supplementation. Clinical avian medicine. vol. 1, Palm Beach: Spix Publishing, 86– 107. Nott H.M.R., Taylor E.J. (1993) Nutrition of Pet Birds. Waltham Book of Companion Animal Nutrition. Oxford: Pergamon Press, 69–84. Randall M.G. (1981) Nutritionally induced hypocalcemic tetany in an Amazon parrot. J Am Vet Med Assoc 179, 1277-1278 Ritchie B.W., Harrison G.J., Harrison L.R. (1994) Nutrition. Avian Medicine: Principles and application. Lake Worth: Wingers publishing, 63-78

Roudybush T.E., Grau C.R. (1991) Cockatiel (Nymphicus hollandicus) nutrition. Journal of Nutrition 121, 11S, S206 Schoemaker N.J., Lumeij J.T., Dorrestein G.M., Beynen A.C. (1999) Voedingsgerelateerde problemen bij gezelschapsvogels. Tijdschrift Diergeneeskunde 124, 39-43 Scott I., Evans P.R. (1992) The metabolic output of avian (Sturnus vulgaris, Calidris alpina) adipose tissue, liver, and skeletal muscle: implications for BMR/body mass relationships. Comp Biochem Physiol. 103, 329–332 Sedgwick C. , Pokras M. , Kaufman G. (1990) Metabolic scaling: Using estimated energy costs to extrapolate drug doses between different species and different individuals of diverse body sizes. Proc Am Assoc Zoo Vet , 249-254 Werquin G.J.D.L., De Cock K.J.S., Ghysels P.G.C. (2005) Comparison of the nutrient analysis and caloric density of 30 commercial seed mixtures (in toto and dehulled) with 27 commercial diets for parrots. Journal of Animal Physiology and Animal Nutrition 89, 215-221 Westfahl C., Wolf P., Kamphues J (2008) Estimation of protein requirement for maintenance in adult parrots (Amazona spp.) by determining inevitable N losses in excreta. Journal of Animal Physiology and Animal Nutrition, 92, 384-389


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