Nutrient Requirements Carnivores

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Duane E. Ullrey

Michigan State University, East Lansing, Michigan, U.S.A.

INTRODUCTION

Carnivores, broadly defined, sustain themselves by feeding on vertebrate or invertebrate animal tissues, a practice observed in both the animal and plant kingdoms. The Venus flytrap (Dionaea muscipula), one of over 500 carnivorous plant species, lives in humid, acidic bogs in the Carolinas and, like most plants, acquires energy and nutrients by photosynthesis and through the roots. In this environment, nitrogen and some mineral elements are in short supply, and these needs are met by capturing insects attracted to nectar in a specialized leafy trap, functioning both as a mouth and stomach. Animals, of course, do not possess roots or the mechanisms of photosynthesis. Thus, energy and nutrient requirements of wild carnivorous animals are acquired principally by consuming vertebrate or invertebrate prey.[1,2]

Wilson[3] estimated there are about 4000 species of extant mammals, 9000 of birds, 6300 of reptiles, 4200 of amphibians, and 18,000 of fish and lower chordates. The nutrient requirements of these species are presumed to be qualitatively similar, but quantitative nutrient requirements have been defined by the National Academy of Sciences/National Research Council (NAS/NRC) only for humans and a few domesticated or captive mammals, birds, and fish. Of the species with NRC-defined requirements, the cat, mink, tarsiers, rainbow trout, and salmon are obligate carnivores. The NRC also has defined the nutrient requirements of the dog and fox, but these species appear to be facultative carnivores and may consume considerable vegetable matter.

CARNIVOROUS MAMMALS

The immediate ancestors of the domestic cat (Felis catus) were strictly carnivorous, and its needs have been the most thoroughly studied of any of the obligate carnivores. Although commercial diets for cats may contain vegetable matter, the nutrients and the amounts that must be present reflect a long evolutionary dependence on a strictly carnivorous diet. The cat has a simple digestive system, presumably because digestibility of natural prey tends to be high, and there is no need for extended food retention and microbial fermentation. Due to its limited ability to conserve nitrogen, the cat has a high protein requirement, and it converts only negligible amounts of tryptophan to niacin (neither ability is necessary when consuming whole prey). Requirements for blood glucose are met primarily by gluconeogenesis rather than from dietary carbohydrate, and the cat has a high requirement for arginine for disposal of nitrogen via the urea cycle. It requires taurine and arachidonic acid because of limited tissue synthesis (vertebrate prey provide adequate amounts), and it is unable to convert b-carotene (a plant provitamin) to vitamin A. Vitamin D3 needs are met by diet because cutaneous concentrations of 7-dehydrocholesterol (provitamin D3) are insufficient to support vitamin D photobiogenesis. Nutrient needs of the cat have been reviewed by the NRC,[4] and minimal requirements, adequate intakes, and recommended allowances have been published. The NRC-recommended allowances for growth, maintenance, late gestation, and peak lactation are presented in Table 1.

The mink (Mustela vison) eats small mammals, fish, frogs, crayfish, insects, worms, and birds in the wild. Like the cat, its protein requirements are high 38% of dietary dry matter (DM) from weaning to 13 weeks of age, 22 26% for adult maintenance, 38% for gestation, and 46% for lactation.[5] Whether the mink shares the other unique metabolic features of the cat has not been determined.

Tarsiers (Tarsius spp.) eat insects (beetles, ants, locusts, cicadas, cockroaches, mantids, moths) and sometimes small vertebrates in the wild. Although the quantitative nutrient requirements of tarsiers have not been specifically defined, estimated adequate nutrient concentrations in dietary DM have been proposed.[6] When kept in captivity, tarsiers are often provided crickets as a major food item. Because crickets and other commercially available insects tend to be deficient in certain nutrients (particularly calcium, vitamin A, and vitamin D),[7] specifically formulated diets are offered to these insects for about 48 hours before feeding them to tarsiers so that the insects plus their gut contents will be nutritionally complete.[8-10]

Other obligate carnivorous mammals include felids such as lions, tigers, leopards, cheetahs, and jaguars. Aquatic mammals such as dolphins, seals, sea lions, and walruses also are obligate carnivores, but little is known about their quantitative nutrient requirements.

Table 1 Recommended nutrient allowances in dietary dry matter (DM) for domestic cats consuming diets containing 4 kcal of metabolizable energy per g of DM

Nutrient

Growth

Maintenance

Late gestation

Peak lactation

Crude protein, %

22.5

20.0

21.3

30.0

Arginine, %

0.96

0.77

1.50

1.50

Histidine, %

0.33

0.26

0.43

0.71

Isoleucine, %

0.54

0.43

0.77

1.20

Methionine, %

0.44

0.17

0.50

0.60

Meth. +cystine, %

0.88

0.34

0.90

1.04

Leucine, %

1.28

1.02

1.80

2.00

Lysine, %

0.85

0.34

1.10

1.40

Phenylalanine, %

0.50

0.50

Phenyl. + tyrosine, %a

1.91

1.53

1.91

1.91

Threonine, %

0.65

0.52

0.89

1.08

Tryptophan, %

0.16

0.13

0.19

0.19

Valine, %

0.64

0.51

1.00

1.20

Taurine, %b

0.04 0.2

0.04 0.2

0.04 0.2

0.04 0.2

Total fat, %

9.0

9.0

9.0

9.0

Linoleic acid, %

0.55

0.55

0.55

0.55

a Linolenic acid, %

0.02

0.02

0.02

Arachidonic acid, %

0.02

0.004

0.02

0.02

Eicosapentaenoic and

0.01

0.01

0.01

0.01

docosahexaenoic acid, %

Calcium, %

0.80

0.29

1.08

1.08

Phosphorus, %

0.72

0.26

0.76

0.76

Magnesium, %

0.04

0.04

0.06

0.06

Sodium, %

0.14

0.07

0.13

0.13

Potassium, %

0.40

0.52

0.52

0.52

Chloride, %

0.09

0.10

0.20

0.20

Iron, mg/kg

80

80

80

80

Copper, g/kg

8.4

5.0

8.8

8.8

Zinc, mg/kg

75

75

60

60

Manganese, mg/kg

4.8

4.8

7.2

7.2

Selenium, mg/kg

0.4

0.4

0.4

0.4

Iodine, mg/kg

2.2

2.2

2.2

2.2

Vitamin A, IU/kg

3,550

3,550

7,500

7,500

Vitamin D3, IU/kg

250

250

250

250

RRR a tocopherol, mg/kg

38

38

38

38

Vitamin K (menadione), mg/kg

1.0

1.0

1.0

1.0

Thiamin, mg/kg

5.5

5.6

5.5

5.5

Riboflavin, mg/kg

4.25

4.25

4.25

4.25

Pyridoxine, mg/kg

2.50

2.50

2.50

2.50

Niacin, mg/kg

42.5

42.5

42.5

42.5

Pantothenic acid, mg/kg

6.25

6.25

6.25

6.25

Folic acid, mg/kg

0.75

0.75

0.75

0.75

Biotin, mg/kg

75

75

75

75

Vitamin B12, mg/kg

22.5

22.5

22.5

22.5

Choline, mg/kg

2,550

2,550

2,550

2,550

aAt least twice as much phenylalanine (or phenylalanine plus tyrosine) is required for maximal black hair color as for growth.

bRecommended taurine allowances are lowest when diets are unprocessed (0.04% of DM) but are increased by extrusion (0.1% of DM) or canning (0.2% of DM).

(Adapted from Ref. 4, recommended allowances for growth of an 800 g kitten, maintenance or late gestation of a 4 kg adult cat, and lactation of a 4 kg queen with four kittens.)

aAt least twice as much phenylalanine (or phenylalanine plus tyrosine) is required for maximal black hair color as for growth.

bRecommended taurine allowances are lowest when diets are unprocessed (0.04% of DM) but are increased by extrusion (0.1% of DM) or canning (0.2% of DM).

(Adapted from Ref. 4, recommended allowances for growth of an 800 g kitten, maintenance or late gestation of a 4 kg adult cat, and lactation of a 4 kg queen with four kittens.)

CARNIVOROUS BIRDS

The digestive systems of obligate carnivorous birds (such as hawks and eagles), like their mammalian counterparts, do not have compartments adapted for microbial fermentation. Relatively indigestible portions of prey, such as fur, feathers, bones, fins, scales, shells, and exoskeletons, may be separated from more digestible portions by the beak prior to food ingestion. Sometimes, this separation is accomplished in the gizzard, followed by egestion of indigestible matter out of the mouth, as in owls.[11] Although the NRC[12] has defined the nutrient requirements of poultry, these species are principally herbivorous. Based on present metabolic evidence and the composition of vertebrate and invertebrate prey, it seems likely that nutrient needs of carnivorous birds are similar to those of carnivorous mammals, with adjustments for differences in reproductive strategy.

CARNIVOROUS REPTILES AND AMPHIBIANS

The long evolutionary association of snakes, crocodilians, and some lizard families with subsistence on vertebrate and invertebrate prey suggests that they are obligate carnivores. They tend to have simple gastrointestinal systems as compared to herbivorous reptiles, although there are adaptations related to the periodicity of feeding and to unique characteristics of certain food items. Tortoises are chiefly herbivorous with a few that are omnivorous. Turtles tend to be omnivorous carnivorous as juveniles and herbivorous or omnivorous as adults although a few species are mostly carnivorous throughout life.[13] Studies that define qualitative or quantitative needs of reptiles are few, although protein and amino acid needs of the hatchling green sea turtle (Chelonia mydas; carnivorous as hatchlings, herbivorous as adults) have been investigated. Some studies suggest that young red-eared slider turtles (Trachemys scripta elegans) and green anoles (Anolis carolinensis) do not have an elevated requirement for arginine (as does the cat), and addition of taurine to a diet based on plant proteins does not improve growth of young American alligators (Alligator missis-sippiensis). Also, American alligators appear to convert linoleic acid to arachidonic acid to some extent, although rates may not be optimum for maximum growth.[1] When a purified diet containing adequate tryptophan but no niacin was administered weekly by stomach tube to bull snakes (Pituophis melanoleucus sayi) for 132 days, no signs of deficiency were seen, suggesting that either a longer period of depletion is necessary to induce niacin deficiency or metabolic conversion of tryptophan to niacin may occur in this species.[14] Thus, if these reptiles are indeed obligate carnivores, their nutrient needs seem to deviate from those of the cat.

Most amphibians appear to be obligate carnivores.[13] Adult frogs and toads consume invertebrates and small vertebrates, although most species are herbivorous as larvae (tadpoles) and have a long, coiled intestine permitting them to digest plant matter. At metamorphosis, the intestine is much shortened and the diet becomes strictly carnivorous. Tadpoles of a few species are carnivorous and have a much shorter gut than do herbivorous tadpoles. Salamanders and newts are carnivorous both as larvae and as adults, feeding on insects, slugs, snails, and worms. Caecilians (limbless, viviparous amphibians) prey on worms, termites, and orthopterans. Metabolic features characteristic of carnivory have not been well studied in amphibians.

CARNIVOROUS FISH

Rainbow trout (Salmo gairdneri) and coho salmon (Oncorhynchus kirsutch) have protein requirements of > 40% of dietary DM for maximal growth of juveniles and have an absolute requirement for arginine. They also lack the ability to synthesize niacin from tryptophan. Gluco-neogenesis is important for provision of blood glucose, and essential fatty acid requirements include linoleic acid and eicosapentaenoic acid and/or docosahexaenoic acid.[15]

CONCLUSIONS

Qualitative and quantitative nutrient requirements of obligate carnivores generally appear to reflect evolutionary adaptations to the composition of ancestral diets.

REFERENCES

1. Allen, M.E.; Oftedal, O.T. The Nutrition of Carnivorous Reptiles. In Captive Management and Conservation of Amphibians and Reptiles, Contributions to Herpetology, Vol. 11; Murphy, J.B., Adler, K., Collins, J.T., Eds.; Society for the Study of Amphibians and Reptiles: Ithaca, NY, 1994; 71 82.

2. Allen, M.E.; Oftedal, O.T.; Baer, D.J. The Feeding and Nutrition of Carnivores. In Wild Mammals in Captivity: Principles and Techniques; Kleiman, D.G., Allen, M.E., Thompson, K.V., Lumpkin, S., Eds.; Univ. Chicago Press: Chicago, IL, 1996; 139 147.

3. Wilson, E. The Diversity of Life; Harvard Univ. Press: Cambridge, MA, 1992.

4. National Research Council. Nutrient Requirements ofDogs and Cats; National Academies Press: Washington, DC, 10. 2004.

5. National Research Council. Nutrient Requirements of Mink and Foxes, 2nd Rev.; National Academy Press: Wash ington, DC, 1982. 11.

6. National Research Council. Nutrient Requirements of Nonhuman Primates, 2nd Rev. Ed.; National Academies 12. Press: Washington, DC, 2003.

7. Finke, M.D. Complete nutrient composition of commer 13. cially raised invertebrates used as food for insectivores. Zoo Biol. 2002, 21, 269 285.

8. Allen, M.E.; Oftedal, O.T. Dietary manipulation of the 14. calcium content of feed crickets. J. Zoo Wildl. Med. 1989, 20, 26 33.

9. Finke, M.D. Gut loading to enhance the nutrient content of insects as food for reptiles: A mathematical approach. Zoo 15. Biol. 2003, 22, 147 162.

Roberts, M.; Kohn, F. Habitat use, foraging behavior, and activity patterns in reproducing Western tarsiers, Tarsius bancanus, in captivity: A management synthesis. Zoo Biol. 1993, 12, 217 232.

Klasing, K.C. Comparative Avian Nutrition; CAB Inter national: New York, NY, 1998.

National Research Council. Nutrient Requirements of Poultry; National Academy Press: Washington, DC, 1994. The Encyclopedia of Reptiles and Amphibians; Halliday, T.R., Adler, K., Eds.; Facts on File, Inc.: New York, NY, 1986.

Bartkiewicz, S.E.; Ullrey, D.E.; Trapp, A.L.; Ku, P.K. A preliminary study of niacin needs of the bull snake (Pituophis melanoleucus sayi). J. Zoo Anim. Med. 1982, 13, 55 58.

National Research Council. Nutrient Requirements of Fish; National Academy Press: Washington, DC, 1993.

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    What nutrient is nonessential for carnivores?
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