Rockhopper Penguin | Photo Credit: Wikimedia Commons by Ben Tubby
The following Penguin Nutrition Guide is taken mostly from the AZA Nutrition Advisory Group’s Document “Penguins: Nutrition and Dietary Husbandry” by Sue Crissey, PhD, Kerri Slifka, MS and Patty McGill, PhD at the Conservation Biology and Research Center, Chicago Zoological Society at Brookfield Zoo.
A summary of the food items consumed by free-ranging penguins is presented in Table 1. All species consume more than one type of food in the wild, generally fish, krill, and/or squid. Penguins that live at lower latitudes, such as little blue penguins and the Spheniscus species, tend to rely much more heavily on fish than do the high-latitude species.10
|Penguin species||Krilla||Squidb||Sardinesc||Round herringd||Pilcharde||Anchoviesf||Lanternfish/ myctophids||Maasbankerg||Mulleth||Icefish/ nototheniids||Fish (various spp.)|
|aEuphausiid crustaceans primarily in genera Euphausia, Thysanoessa, and Nyctiphanes.|
|bCephalopods in genera Loligo, Heteroteuthis, Argonauta, Nototodarus, Sepioteuthis, Teuthowenia, Psychroteuthis, Alluroteuthis, Kondakovia, Gonatus, Todarodes, Moroteuthis, and Loligunculus.|
|eSardinops ocellata, S. neopilchardus|
|fEngraulis capensis, E. australis, E. ringens|
Nutrient Requirements and Related Concerns
The following information on nutrient requirements and nutrient content of food items is presented on a dry matter basis (DMB). Dry matter (DM) concentrations in whole fish and marine invertebrates range from about 14-37%.2
Published nutrient data
There are insufficient data from research with penguins to set nutrient requirements with certainty. Despite consumption of a variety of prey in the wild, it is likely that all penguin species have similar qualitative nutrient needs. It also is likely that the nutrient requirements of penguins are qualitatively similar to the nutrient requirements of most birds and mammals. The National Research Council (NRC) has published estimated nutrient requirements of domestic birds 31 and the carnivorous domestic cat.29 Using these NRC estimates as guidelines, plus data on nutrient composition of free-ranging penguin foods and foods available in captivity, minimum nutrient concentrations in diets for captive penguins are proposed in Table 2. These levels should be considered tentative until more specific nutrient requirements for penguins are defined.
Table 2. Proposed minimum energy and nutrient concentrations (DMB) in adult penguin dietsa based on requirements of domestic poultry,31 cats,29 and inferences from composition of wild foods.2
|Gross energy, kcal/g||4.5|
|Crude Protein, %||35|
|Vitamin A, IU/kg||3,500|
|Vitamin D, IU/kg||500|
|Vitamin E, IU/kg||400b|
|a Other nutrients, such as essential fatty acids, essential amino acids, Vitamin K, and the other B-complex vitamins are probably required. Nevertheless, there is no evidence that inadequate concentrations are provided by fish and marine invertebrates. Whether vitamin C can be synthesized by penguin tissues has not been established. Freshly caught fish contain significant concentrations of this vitamin, and some destruction undoubtedly occurs during storage. However signs of vitamin C deficiency in the penguin have not been described.|
|b Although this concentration of vitamin E may exceed the minimum requirement, about 400IU/kg of DM provided by the supplement of 100 IU of vitamin E/kg of fresh fish is recommended to compensaite for losses during peroxidation of unsaturated fatty acids.|
|c This concentration of thiamin undoubtedly exceeds the minimum requirement, but about 100-120 mg/kg of DM are provided by the supplement of 25-30 mg of thiamin/kg of fresh fish to compensate for destruction by thiaminases.|
Penguins obtain water from food as well as in liquid form.23,33,37 Because of their nasal salt glands, penguins are able to consume salt water.33 However, in captivity, fresh water is commonly provided to meet possible needs beyond the water from food. If penguins have access only to fresh water, extra salt has sometimes been added to the diet to ensure development and maintenance of nasal salt gland function.12 Whether this is a necessary practice has not been established.
It is presumed that penguins eat to meet their energy needs and will consume a greater mass of less energy-dense foods than of energy-rich foods. Gut-fill limits should not be a problem, given the relatively high energy density of most fish and the penguin’s considerable stomach capacity. Penguins have been reported to carry up to 20-30% of their body mass in their stomachs as they bring food to their chicks.10
Alterations in energy intake are associated with molt.17 There are several cues that induce this process, including changes in ambient temperature, day length, food resource availability (and possibly food nutrient content), and associated hormonal changes.17 It appears that if fed an adequate diet ad libitum and the environment accurately mimics seasonal light and temperature changes, most captive penguins will exhibit a normal annual cycle of food intake and will molt and reproduce normally.26,41
Adelie Penguin feeding young | Photo Credit: Wikimedia Commons
Vitamins and minerals.
Mazuri makes a Fish Eater Tablet containing vitamins and minerals required by fish-eating birds such as penguins.
Dietary vitamin A requirements for studied avian species are between 1,700 and 5,600 IU/kg of diet on a DM basis.31 Based on limited data, the vitamin A requirement for cats is 6,000 IU/kg of dietary DM.29 It is possible that penguins, as fish-eating birds, have a high tolerance for vitamin A because comparatively high levels occur in their natural diet.9 Whether this infers a high dietary vitamin A requirement has not been established.
Vitamin D3 requirements for most adequately studied bird species are between 220 and 1,000 IU/kg of diet on a DM basis.31 Cats have a vitamin D3 requirement of about 500 IU/kg of dietary DM.29 Data on vitamin D3 concentrations are available for very few penguin foods, but two species of smelt and one species of krill were found to have <633 IU/kg DM.2 Atlantic mackerel, capelin, herring, and whitebait had vitamin D3 concentrations that were much higher, ranging from 2,500 IU/kg DM in the latter to 16,800 IU/kg DM in the former.
Vitamin E is destroyed over time in stored marine foods.2 It has been proposed that foods for marine animals should be supplemented with 100 IU of vitamin E/kg of diet on a wet basis or approximately 400 IU/kg DM.15
Thiaminases have been identified in mackerel, herring, smelt, and clams with activity sufficient to destroy much of the tissue Thiamin during frozen storage.2 It has been proposed that thiamin supplements should be added to marine animal diets, providing 25-30 mg/kg diet on a wet weight basis or approximately 100-120 mg/kg DM.15
Calcium concentrations in whole fish and krill (0.9-6.4% of DM)2 seem adequate, even for breeding and laying penguins, and calcium supplements should not be required. Squid, however, are relatively low in calcium (0.1-0.2% of DM) and have an inverse calcium:phosphorus ratio. Some institutions have reported problems (without dietary details) in captive penguins that were ascribed to calcium deficiency during production of multiple clutches, and calcium supplements were used with no apparent ill effect.12 However, consideration should be given to the concentrations of calcium, phosphorus, and vitamin D in dietary items (using analyses, if necessary), and to calcium:phosphorus ratio, since a disproportionate supply of one of these nutrients can adversely influence metabolism of the others.
Sodium is an essential nutrient for all animals. It is thought by some that the requirement for sodium is a special consideration for functional development of the nasal glands of marine birds with access only to fresh water.12 Some institutions, with both fresh and saltwater environments, supplement penguin diets with salt at approximately 250 mg of NaCl/bird/day, without apparent harm.12 The necessity for this practice has not been established, and it is noteworthy that the fish and invertebrates that have been analyzed, whether of marine or freshwater origin, contain sodium concentrations (0.2-5.5% of DM)2 that are higher than the minimum need of any species for which a requirement has been established.
Based on analytical values for other nutrients in fish and marine invertebrates, it seems unlikely that other deficiencies would appear unless unwise food choices have been made or storage and handling of these foods has been below standards.8
Vitamin excesses. Fat-soluble vitamins A, D, and E accumulate in the body when intakes exceed need, and excessive amounts over extended periods will produce signs of toxicity.25 It should be noted, however, that there are seasonal differences in the availability of these vitamins for some animal species in the wild, and the accumulation of body stores during comparatively short natural periods of plenty may be critical for health during periods of short supply. Chronic vitamin A toxicity typically results from long-term intakes that are 100 to 1,000 times dietary requirements, although toxic signs have been reported from dietary levels as low as 10 times the requirement.30
The most characteristic signs of chronic vitamin A toxicity include skeletal malformations associated with excessive bone remodeling, spontaneous fractures, and internal hemorrhage. Other signs include anorexia, slow growth, weight loss, impaired liver and kidney function, enteritis, conjunctivitis, suppression of keratinization, and thickened skin. Elevated serum levels of vitamin A have been observed in captive Humboldt penguins fed diets containing 59,800 IU of vitamin A/kg (DMB) for 12 months, but no toxicity signs were seen.9
Birds and many mammals appear to utilize vitamin D3 more efficiently than vitamin D2, and vitamin D3 is about 10 to 20 times more toxic.30 Recommended maximum tolerable limits for long-term consumption by species that have been studied are about 4 to 10 times the requirement.30 Signs associated with chronic vitamin D toxicity include anorexia, hypercalcemia, hypercalciuria, and calcification of soft tissues, especially kidneys, aorta, and lungs. There have been no reports of vitamin D toxicity in penguins.
Maximum tolerable levels of dietary vitamin E are quite high, but interference with blood clotting has been reported in pelicans with supplements of vitamin E adding 1,000 to 2,000 IU/kg of dietary DM.32 Elevated serum levels of vitamin E have been observed in captive Humboldt penguins fed diets containing 58,600 IU of vitamin E/kg (DMB) for 12 months, but there were no signs of toxicity.9
Vitamin K has a relatively short metabolic half-life, and toxicity has not been demonstrated when large quantities of vitamin K were provided in a natural form such as phylloquinone. Furthermore, toxic dietary levels of menadione and its derivatives are at least 1,000 times the vitamin K requirement.30
Potential Penguin Foods and Their Nutrient Composition
Potential penguin foods
Several diets currently fed to penguins are presented in Table 3. Frozen fish and marine invertebrates are available from a number of commercial suppliers. Some are purveyors of human food but also sell to zoos and aquariums. Others serve the zoo and aquarium market exclusively. Regardless, the quality of products purchased for feeding to penguins should meet human food standards.8 The supplier should use a Hazard Analysis Critical Control Point (HACCP) program to help ensure that fish and marine invertebrates have been handled appropriately.8
Table 3. Penguin diets from selected zoos. Amounts are per bird, per day, as fed.
|Penguins and zoo||Capelin||Herring||Lake Smelt||Krill||Marine Smelt||Surf Smelt||Vitamin E (IU)||Thiamin (mg)||Multivitamin||NaCl (g)||Cod liver oil (tsp)|
|Brookfield||341g||170g||170g||100||25||0.4g Windmill Daily Max. Form.|
|Sea World Orlando||2-3lb of mixed fisha||+b||250||1 Mazuri Vita-Zu Mammal Tabletc|
|Sea World Orlando||1-1.5lb mixed fisha||+b||250||1 Mazuri Vita-Zu Large Bird Tabletc|
|Sea World Orlando||1.5-2lb mixed fisha||+b||250||1 Mazuri Vita-Zu Large Bird Tabletc|
|Sea World Orlando||2-2.5lb mixed fisha||+b||1 Mazuri Vita-Zu Large Bird Tabletc|
|Sea World Orlando||1.5-2lb mixed fisha||+b||1 Mazuri Vita-Zu Large Bird Tabletc|
|a All species of penguins are fed a mix of capelin, large herring, lake smelt, and krill. Average total amount consumed is noted.|
|b Vitamin E provided in the Mazuri Vita-Zu Large Bird and Mammal Tablets|
|c Sea World Orlando also supplements with calcium gluconate at 650mg (1 10-grain tablet) Setp-Dec for King penguins and 325mg (1/2 10-grain tablet) Sept-Nov for Rockhopper, Chinstrap, Magellanic and Gentoo penguins.|
Given the current status/depletion of wild fish stock, suppliers should be encouraged to practice sustainable-use fishing. Successful captive penguin husbandry depends upon a consistent source of high quality food that the penguins will eat. Because certain prey species are not available year-round, it may be necessary to purchase quantities sufficient for several months to ensure an uninterrupted supply. This necessitates that penguin foods be properly frozen and stored until used. Given the perishable nature of seafood, appropriate storage and handling procedures are crucial. These include freezing as soon as possible after catching and frozen storage that maintains an average product temperature of -18 to -30 C. Stock rotation should be practiced to ensure that foods are not stored for more than 4 -6 months. Frozen foods should be thawed under refrigeration at temperatures of 2-3.5 C, as close in time as possible to feeding. See NAG Fact Sheet 005 “Feeding Captive Piscivorous Animals: Nutritional Aspects of Fish as Food”2 and USDA publication “Handling Fish Fed to Fish-Eating Animals: A Manual of Standard Operating Procedures” 8 for additional details on freezing, storage, and thawing.
The nutrient composition of fish and marine invertebrates fed to captive piscivorous animals has been discussed by Bernard and Allen in NAG Handbook Fact Sheet 005.2 Dry matter, crude protein, crude fat, gross energy, mineral, and fat-soluble vitamins A, D, and E concentrations in common fish and marine invertebrates are presented in that report. These values vary with species, age, gender, physiologic state, and season and locale of harvest.
Dry matter. Dry matter concentrations range from about 14-37% in penguin foods, so water intakes would be 2-6 times higher than dry matter intakes when these foods are consumed. If metabolic water from tissue oxidation of absorbed food or stored fat is added to the water in food, there may be little need for consumption of liquid water. However, definitive studies on water requirements of penguins in captivity have not been conducted.
Crude protein. Crude protein concentrations, on a DMB, range from about 33-77%. Amino acid requirements of penguins are unknown. Since penguins consume whole fish or marine invertebrates, a specific amino acid deficiency is unlikely. 23
Crude fat. Crude fat concentrations, on a DMB, range from about 8 -48% and tend to be inversely related to protein concentrations.1
Minerals. Ash concentrations range from 5-24%, on a DMB, are low in invertebrates, and are related to the proportion of bone in fish. Essential mineral concentrations in fish appear to be sufficient, although a few fish have relatively low concentrations of copper and manganese. Calcium concentrations in squid are likely to be inadequate, if used as a sole source of food. However, the mineral requirements of penguins have not been determined.
Fat-soluble vitamins. Concentrations of fat-soluble vitamins A, D, and E in freshly caught fish are probably adequate for penguins, and in some fish species, vitamin A and D levels are very high. However, as previously noted, vitamin E undergoes destruction during storage, and supplemental vitamin E should be provided. Vitamin K concentrations in whole fish have not been reported, but signs of deficiency in penguins are unlikely unless induced by feeding excesses of vitamins A or E.
Water -soluble vitamins. It is unlikely that supplements of water-soluble vitamins, except for thiamin, are required when whole fish and squid are fed.
It is generally accepted that captive penguins have food preferences. The types and species of prey available for captive feeding are limited and may be quite different from the variety with which penguins evolved. Even data from free-ranging penguins suggest that the food items most consumed may not be those most preferred but may be foods that are most available.20,21 Differences in food choice also may be influenced by physiologic circumstances, such as stage of the reproductive cycle. Selection of particular food items may be an expression of food preference, but, lacking historical and long-term association with those foods, captive penguins appear not to make choices on the basis of nutritional wisdom. Food refusal, on the other hand, may be an indication of spoilage, and if fish are refused, their quality should be checked. Ultimately, the responsibility for provisioning captive penguins with nutritionally adequate and healthful food is ours. To avoid dependence on a particular food item, it is prudent to offer a variety. If a penguin becomes “imprinted” on a specific food item and if that item becomes unavailable, it may be difficult to coax acceptance of an alternative. In addition, offering a variety of foods will help ensure that the diet provides a complementary and complete nutrient profile.
The recommended method of feeding is to hand-feed individual penguins, particularly when offering fish that have been injected with nutrient supplements or in which supplement tablets or capsules have been placed. This ensures that each bird will receive intended nutrients and allows the keeper to monitor food and energy consumption. Methods of self-feeding are sometimes used, but keepers should ensure that food items remain cool and clean and are consumed within a short time after being thawed. In exhibits held at or below 4°C, fish may be offered in feeding trays for several hours as long as birds are not defecating nor walking in the trays. However, fish should not be left in standing water because of the potential for nutrient loss.
Adult penguins are commonly fed to appetite early in the morning and late in the afternoon, although the number of feedings may be increased during pre-molt and breeding. Appetite usually increases during the pre-molt period and decreases during molt. In a study with captive rockhopper penguins, all birds gained about 23-38% in body mass just prior to molting.26
Among the penguin species that have been studied, most will fast during incubation and molting. In the wild, mean loss of body mass during molt is as much as 40% in macaroni penguins and 47% in king penguins.6,16 During molt in captivity, losses can be as much as 50% of body mass. After these periods, penguins consume vast quantities of food and deposit considerable body fat and protein.16
There is no need to limit food intake below ad libitum levels unless the penguin is extremely overweight. An average captive but active adult penguin’s daily food consumption on an as-fed basis is approximately 2 -3% of body mass for the larger species, such as kings and emperors (Aptenodytes forsteri), and 10-14% for smaller species, such as Humboldts and rockhoppers.12 However, the specific quantities consumed depend on the activity level and physiologic state of the individual.
The size of food items offered should be appropriate for easy manipulation and swallowing. Purchasing specifications for fish and squid should include size designations so that they can be fed whole. Whole food is accepted most readily, but if it must be cut because it is too large, all portions should be fed to ensure that the entire supply of nutrients contained in the whole food will be consumed. Lengths of fish consumed by free-ranging adult emperor penguins were 60 to 120 mm (~2.5-5 in), and lengths of squid consumed were 19 to 280 mm (<1-11 in).
Formulation of Appropriate Diets
When formulating diets for captive penguins, flexibility is needed to account for variations in food preferences, body mass, activity, physical condition, environment, and behavior, as well as food availability and nutrient content.
Marine fish versus fresh-water fish
Historically, most captive penguins have been fed marine fish. Given current problems with commercial fish availability, it is becoming more common to offer fresh-water fish, as well. This trend may continue as commercial fresh-water fish farms increase in number and the yield from marine fisheries declines. Although fresh-water fish may be used, it may be prudent to also feed one or more species of marine fish.
Many institutions supplement with a variety of multivitamins and minerals. This is presumably to provide for any possible losses due to storage, thawing, or to ensure that these nutrients are always present on a daily basis regardless of fish offered. Several products are marketed specifically for marine animals but differ in composition. If a variety of high quality fish are fed, and if they are stored and thawed properly, it is unlikely that supplements, other than of vitamin E and thiamin, will be needed. Thiamin can be purchased in tablets and vitamin E in capsules. They can be hidden inside the mouth or gills of fish, and the supplemented fish hand-fed to individual penguins. Alternatively, solutions or suspensions of these vitamins can be injected into fish and the injected fish hand-fed. Supplements of 25-30 mg of thiamin and 100 IU of vitamin E should be provided for each kg of food (wet basis). Adjustments in the amounts of supplement provided should be made in proportion to the mass of food consumed. .
Parent Rearing of Chicks
The most important dietary adjustment, when chicks are being reared by their parents, is to offer enough fish to the parents so they may adequately feed themselves and their offspring. During chick rearing, parents should be fed ad libitum and frequently.
Literature Cited from above document:
1 Ackman R. G., and J. Kean-Howie. 1994. Fatty acids in aquaculture: are omega-3 fatty acids always important? Pp. 82-103 in Lim, C., and D.J. Sessa (eds.). Nutrition and Utilization Technology in Aquaculture. Am. Oil Chem. Soc. Press, Champaign, IL.
2 Bernard J.B., and M.E. Allen. 1997. Feeding Captive Piscivorous Animals: Nutritional Aspects of Fish as Food. Nutrition Advisory Group Handbook Fact Sheet 005. Publ. by Chicago Zoological Society, Brookfield Zoo, Brookfield, IL
3 Bost, C.A., P. Koubbi, F. Genevois, L. Ruchon, and V. Ridoux. 1994. Gentoo penguin Pygoscelis papua diet as an indicator of planktonic availability in the Kerguelen Islands. Polar Biol. 14:147-153.
4 Burger, I. 1993. The Waltham Book of Companion Animal Nutrition. Pergamon Press, New York, NY.
5 Cherel, Y., and V. Ridoux. 1992. Prey species and nutritive value of food fed during summer to King penguin Aptenodytes patagonicus chicks at Possession Island, Crozet Archipelago. Ibis 134:118-127.
6 Cherel Y., J.B. Charrassin, and E. Challet. 1994. Energy and protein requirements for molt in the King penguin, Aptenodytes patagonicus. Am. J. Physiol. 266:R1182-R1188.
7 Cherel, Y., R. Mauget, R. Lacroix, and J. Gillis. 1994. Seasonal and fasting-related changes in circulating gonadal steroids and prolactin in King penguins (Aptenodytes patagonicus). Physiol. Zool. 67:1154-1173.
8 Crissey, S.D. 1998. Handling Fish Fed to Fish-Eating Animals: A Manual of Standard Operating Procedures. U.S. Dept. Agr., Agr. Res. Serv., Natl. Agr. Libr., Beltsville, MD.
9 Crissey, S.D., P. McGill, and A.M. Simeone. 1998. Influence of dietary vitamins A and E on serum alpha- and gamma-tocopherols, retinol, retinyl palmitate and carotenoid concentrations in Humboldt penguins Spheniscus humboldti. Comp. Biochem. Physiol. Part A 121:333-339.
10 Croxall, J. P., and G.S. Lishman. 1987. Food and feeding ecology of penguins. Pp. 101-133 in Croxall, J.P. (ed.). Seabirds: Feeding Ecology and Role in Marine Ecosystems. University of Cambridge Press, Cambridge, MA.
11 Cullen, J.M., T.L. Montague, and C. Hill. 1992. Food of little blue penguins, Eudyptula minor, in Victoria: comparison of three localities between 1985 and 1988. Emu 91:318-341.
12 Ellis, S., and S. Branch (eds.) 1994. Penguin Husbandry Manual, 1st Ed. Beall, F., S. Branch, A. Cramm, S. Crissey, S. Ellis, L. Henry, P. McGill, T. Schneider, G. Sirpenski, and M. Walsh. Amer. Zoo and Aquarium Assoc., Bethesda, MD.
13 Engelhardt, F.R., and J. R. Geraci. 1978. Effects of experimental vitamin E deprivation in the harp seal, Phoca groenlandica. Can. J. Zool. 56:2186-2193.
14 Geraci, J.R., and D. J. St. Aubin. 1980. Nutritional disorders of captive fish-eating animals. Pp. 41-49 in Montali, R.J., and G. Migaki (eds.). The Comparative Pathology of Zoo Animals. Smithsonian National Press, Washington, DC.
15 Geraci, J.R. 1986. Marine mammals (cetacea, pinnipeds, and sirenia): nutrition and nutritional disorders. Pp 760-764 in Fowler, M.E. (ed). Zoo and Wildlife Medicine (2nd Ed.). W.B. Saunders Co., Philadelphia, PA.
16 Ghebremeskel, K., T.D. Williams, G. Williams, D.A. Gardner, and M.A. Crawford. 1991. Plasma metabolites in Macaroni penguins Eudyptes chrysolopus arriving on land for breeding and molting. Comp. Biochem. Physiol. 99A:245-250.
17 Ghebremeskel, K., T.D. Williams, G. Williams, D.A. Gardner, and M.A. Crawford. 1992. Dynamics of plasma metabolites in molting Macaroni Eudyptes chrysolophus and Gentoo penguins Pygoscelis papua. Comp. Biochem. Physiol. 101A:301-307.
18 Griffin, M., W.C. Sadler, D.C. Salmon, and K. Wright. 2000. PB and J: Gelly was never like this. Proc AAZV and IAAAM Joint Conference. New Orleans, LA.
19 Hays, C. 1984. The Humboldt penguin in Peru. Oryx 18:92-95.
20 Hays, C. 1986. Effects of the 1982-83 El Niño on Humboldt penguin colonies in Peru. Biol. Conserv. 36:169-180.
21 Hobday, D.K. 1992. Abundance and distribution of pilchard and Australian anchovy as prey species for the Little Blue Penguin Eudyptula minor at Phillip Island, Victoria. Emu 91:342-354.
22 Holland, B., A.A. Welch, I.D. Unwin, D.H. Buss, A.A. Paul, and D.A.T. Southgate. 1992. McCance and Widdowson’s The Composition of Foods, 5th Ed. Royal Society of Chemistry, Cambridge, UK.
23 Lie, Ø., E. Lied, A. Maage, L.R. Njaa and K. Sandnes. 1994. Nutrient content in fish and shellfish. Fisk. Dir. Skr. Ser. Ernaering 6(2):83-105.
24 Lishman, G.S. 1985. The food and feeding ecology of Adelie penguins, Pygoscelis adeliae, and chinstrap penguins, Pygoscelis antarctica, at Signy island, South Orkney Islands. J. Zool. London 205(A):245-263.
25 Machlin, L. J. 1984. Handbook of Vitamins: Nutritional, Biochemical and Clinical Aspects. Marcel-Dekker, Inc., New York, NY.
26 Monroe, A. 1993. Annual variations in plasma retinol and alpha-tocopherol levels in Gentoo and Rockhopper penguins. Zoo Biol. 12:453-485.
27 Montague, T.L. 1982. The food and feeding ecology of the little blue penguin, Eudyptula minor, at Phillip Island, Victoria, Australia. M.Sc. Thesis, Monash Univ.162.
28 Nagy, K.A., and B.S. Obst. 1992. Food and energy requirements of Adelie penguins, Pygoscelis adeliae, on the Antarctic peninsula. Physiol. Zool. 65:1271-1284.
29 National Research Council. 1986. Nutrient Requirements of Cats, Rev. Ed. National Academy Press, National Academy of Sciences, Washington, DC.
30 National Research Council. 1987. Vitamin Tolerances of Animals. National Academy Press, National Academy of Sciences, Washington, DC.
31 National Research Council. 1994. Nutrient Requirements of Poultry, 9th Rev. Ed. National Academy Press, National Academy of Sciences, Washington, DC.
32 Nichols, D.K., M.J. Wolff, L.G. Phillips, and R.J. Montali. 1989. Coagulopathy in pink-backed pelicans, Pelecanus refescens, associated with hypervitaminosis E. J. Zoo Wildl. Med. 20:57-61.
33 Peaker, M., and J.L. Linzell. 1975. Salt Glands in Birds and Reptiles. Cambridge University Press, New York, NY.
34 Putz, K ., and C.A. Bost. 1994. Feeding behavior of free-ranging king penguins ( Aptenodytes patagonicus). Ecology 75:489-497.
35 Rand, R.W. 1960. The biology of guano-producing seabirds. The distribution, abundance, and feeding habits of the Cape penguin, Spheniscus demersus, off the south-western coast of the Cape province. Invest. Reports Div. of Fisheries, South Africa 41:1-28.
36 Robertson, G., R. Williams, K. Green, and L. Robertson. 1993. Diet composition of Emperor penguin chicks Aptenodytes forsteri at two Mawson Coast colonies, Antarctica. Ibis 136:19-31.
37 Slifka, K.A., S.D. Crissey, and J. Goffron. 1997. Fish composition: effects of preparation and analytical methods. Proc. AZA Nutrition Advisory Group Second Conference, Ft. Worth, TX
38 Watanuki, Y., Y. Mori, and Y. Niato. 1994. Euphausia superba dominates in the diet of Adelie penguins, Pygoscelis adeliae, feeding under fast sea-ice in the shelf areas of Enderby Land in summer. Polar Biol. 14:429-432.
39 Williams, T.D. 1991. Foraging ecology and diet of Gentoo Penguins Pygoscelis papua at South Georgia during winter and an assessment of their winter prey consumption. Ibis 133:3-13.
40 Williams, T.D., D.R. Briggs, J.P. Croxall, Y. Naito, and A. Kato. 1992. Diving pattern and performance in relation to foraging ecology in the gentoo penguin, Pygoscelis papua. J. Zool. London 227:211-230.
41 Wilson, R. P. 1985. Seasonality in diet and breeding success of the jackass penguin Spheniscus demersus. J. Ornithol. 126:53-62