Milk Composition Species Comparisons

Olav T. Oftedal

Smithsonian Institution, Washington, D.C., U.S.A.

INTRODUCTION

All mammals depend on milk as their primary source of nutrients during a phase of development. This may begin at an early developmental stage and cover a long period, as in hatchling monotremes or neonatal marsupials, or it may be a brief period following the birth of large, precocial offspring. Milk composition can change markedly during lactation, especially in monotremes and marsupials. These changes probably correlate to developmental maturation in digestive function, substrate metabolism, and requirements for tissue synthesis, but the specifics are not well understood. Milk also provides immunoglobulins and other antibacterial compounds important in protecting suckling young from infection. In this article, the major constituents of milk are discussed, both in terms of significance for the young and in relation to species differences. Examples of the milk composition of a wide variety of species are given.

MAJOR MILK CONSTITUENTS

The most abundant constituents in milk are water, lipids, proteins, and sugars.[1-3] At midlactation, the milks of domesticated and semidomesticated animals used for human consumption range in energy content from 2.1 to 6.9 kJ/g, with most at the lower end (Table 1). Among wild animals a greater range of energy content (1.8 25 kJ/g) is evident, with large differences among mammalian orders as well as among species within an order (Table 2).

Water

Water is essential to neonates for tissue growth and to replace water lost through evaporation and excretion. Milk water ranges from 90% in some zebras, rhinos, and primates to about 30% in some seals (Tables 1 and 2). High water intake may be essential for offspring of zebras and rhinos that require water for evaporative cooling in hot, arid environments. The milks consumed by hatchling monotremes and newborn marsupials are also very high in water (88 91%), which may relate to immature renal function and inability to concentrate urine. Altricial (immature) eutherian neonates also have limited ability to regulate water excretion.

Species that fast during lactation, such as hibernating bears, some seals, and some whales, produce milks that are low in water (30 65%) and thus do not impose a heavy water demand on lactating females. A low water content is also typical of mammalian species that are very small (e.g., shrews, mice), that suckle infrequently (e.g., tree shrews, rabbits), or that live in marine environments (e.g., dolphins, sea otters).

Milks that are high in water are low in energy (Tables 1 and 2), and must be produced in large volumes to meet the energetic needs of suckling young. It is remarkable that most animal milks consumed by humans, such as those of cow, goat, sheep, water buffalo, yak, camel, horse, and ass, are high in water content (82 91%; Table 2). This may reflect a preference for domestication of species that produce larger milk volumes, or it may relate to the fact that human milk is also dilute (Table 1).

Lipids

Milk fat is usually the next most abundant constituent, ranging from less than 1% in rhinos and some lemurs to 50 60% in many seals (Table 2). Milk fat is composed primarily of fatty acids esterified as triacyl glycerols (97 99% by weight) and is packaged in fat globules enveloped in cell membrane, forming a more or less stable emulsion. Given the high energy in lipids, milk fat supplies a large proportion (35 90%) of the energy in most milks, except for equids and rhinos (5 25%).[2]

High-lipid, energy-dense milks may have evolved to support a variety of functions:

• Fat deposition in subcutaneous blubber layers may be necessary for insulation in marine mammal young, such as seals and whales;

• A high energy intake may be needed to fuel high rates of metabolism, as in sea lions and sea otters;

• Mothers may need to transfer energy-dense milks quickly to their young during suckling bouts that are short and infrequent, as in rabbits and tree shrews;

• Mothers that undertake long foraging trips may need to store energy-dense milk in mammary glands between returns to the rookery, as in fur seals and some bats;

• Production of high-fat, low-sugar milk minimizes the glucose demand of lactation for fasting mothers, as in hibernating bears and fasting seals.

Table 1 Major constituents of milks used for human consumption

Days

Gross energya

Water

Fat

Proteinb

Sugar

Protein energy

Species

after birth

kJ/g

(%)

(%)

(%)

(%)

%

Horse

24 54

2.1

89.5

1.3

1.9

6.9

22

Ass

30 180

2.3

89.2

1.8

1.7

6.9

18

Domestic goat

14 56

2.9

88.0

3.8

2.9c

4.7

22

Cow

''mature''

3.0

87.6

3.7

3.2

4.6

26

Zebu

''mature''

3.3

82.7

4.7

3.2

4.9

21

Camel (dromedary)

?

3.4

86.4

4.5

3.6

5.0

26

Bactrian camel

23 91

3.5

84.8

4.3

4.3

30

Human

>10

3.8

87.6

4.1

0.8

6.8

7

Water buffalo

30

4.3

83.2

6.5

4.3c

4.9

23

Sheep

13 35

4.6

81.8

7.3

4.1

5.0

22

Yak

?

4.6

82.7

6.5

5.8c

4.6

30

Eland

30 60

6.0

78.1

9.9

6.3

4.4

32

Reindeer

21 30

6.9

73.7

10.9

9.5c

3.4

32

aEnergy calculated as in Ref. 2. bProtein is protein nitrogen x 6.38. cProtein is total nitrogen x 6.38. (From Refs. 1 3.)

aEnergy calculated as in Ref. 2. bProtein is protein nitrogen x 6.38. cProtein is total nitrogen x 6.38. (From Refs. 1 3.)

Milk fat supplies a source of essential and nonessential fatty acids that are utilized in tissue deposition and metabolism. The fatty acid composition of milk varies greatly among species, reflecting differences in maternal diet, hydrogenation of lipids during digestion, postab-sorptive modification of chain length and double bonds, and de novo synthesis.[5] Ruminant milks are typically rich in short-chain and saturated fatty acids, elephant milks are particularly high in medium-chain (C8 C12) fatty acids, horse milks contain an abundance of unsaturated long-chain (C18) fatty acids, and the milks of pinnipeds (seals and sea lions) and cetaceans (whales and dolphins) are typically high in polyunsaturated, very long chain (C18 24) fatty acids.[5] Milk also contains free and esterified cholesterol as well as a variety of phos-pholipids and glycolipids that may function as metabolic substrates, precursors for structural materials, or protective agents in suckling young.

Proteins

Milk proteins are of central importance because they provide a source of amino acids for suckling young, and serve a variety of functions both in the mammary gland and in suckling young. At midlactation, protein ranges from about 1% to 12% among most species (Table 2), although cottontail rabbit milk may be up to 15%.[3] Protein is usually higher in milks that are rich in lipids, so that the amount of energy supplied as protein is about 20 35% in most taxa (Table 2). However, lower values appear to be characteristic of many seals and sea lions, bats, and primates (Table 2). In primates, the protein-energy percentage is correlated to rate of growth of the young, but this relationship does not hold for all mammals.[6]

The proteins in milk are divided into two categories: caseins and whey proteins.[1] The caseins are organized into large micelles suspended in milk and serve to transport much of the calcium and phosphorus that the young need. Upon ingestion and exposure to gastric secretions, the caseins precipitate in the stomach forming semisolid curds that are gradually digested. It is thought that species that nurse infrequently may have higher casein levels to retain milk constituents in the stomach for longer periods. Cow's milk is higher in casein and forms a more solid curd than does the milk of humans or pigs, which suckle frequently, but few species have been compared in this light.

The whey proteins include milk-specific proteins, such as a-lactalbumin, b-lactoglobulin, and late lactation protein, as well as more widely expressed proteins such as serum albumin, g-globulins, and transferrin.[1,7] Some of these proteins transport trace elements or vitamins, others have enzymatic activity, and some have structural roles in the cell membranes surrounding milk fat globules. The particular set of whey proteins varies among species, and, in some marsupials, may vary according to lactation stage.

Sugars

Lactose is the predominant sugar in the milks of most eutherian mammals, including milks consumed by humans. However, the milks of some marine mammals are devoid of lactose, while a large variety of oligosac-charides are important constituents in the milks of

Table 2 Major constituents of the milks of wild mammals, demonstrating variation within and between ordersa

Gross

Protein

Days

energyb

Water

Fat

Proteinc

Sugar

energy

Sourced

Species

N

after birth

kj/g

(%)

(%)

(%)

(%)

%

Artiodactyla

Collared peccary

4

21 48

3.8

83.8

4.2

5.1

6.2

31

3

Giraffe

12

14 109

5.3

81.5

8.4

5.2

5.3

23

DZ

Bongo

5

15 39

8.0

69.6

13.0

10.4

3.2

31

DZG

Carnivora

Red fox

3

28 35

4.6

81.9

5.8

6.7

4.6

34

2

Giant panda

13 +

77 196

8.6

68.1

15.9

8.1

3.6

22

BU

California sea lion

9

3 60

14.3

59.0

31.7

8.6e

0.3

15

3

Hooded seal

15

24

24.6

30.2

61.1

4.9

1.0

5

3

Cetacea

Fin whale

7 9

~ 210

15.6

53.5

33.2

10.5

2.3

16

3

Chiroptera

Little golden mantled

25

7 11

3.8

87.3

6.1

2.1

6.0

12

9

flying fox

Little brown bat

3

~ 13 19

8.7

72.9

15.8

8.5

4.0

23

3

Brasilian free tailed bat

21

22 42

12.2

63.5

25.8

7.7

3.4

15

3

Marsupialia

Queensland ringtail possum

20 23

100 120

4.3

77.0

3.0

4.5

12.5

24

3

Red necked wallaby

8 39

226

6.2

75.0

7.2

6.8

10.9

26

3

Virginia opossum

5

~ 77

9.7

66

17

10

5.0

25

10

Perissodactyla

Black rhinoceros

8

36 115

1.8

90.0

0.85

1.7

6.6

19

MCZG

Mountain zebra

7

90 360

1.9

90.0

1.0

1.6e

6.9

20

3

South American tapir

9

4 20

3.3

84.8

3.6

4.8

5.0

33

CZS

Primates

Pygmy chimpanzee

9

46 126

1.9

89.6

1.1

1.0

8.0

9

MCZG

Brown lemur

6

28 74

2.1

90.4

0.9

1.3e

8.5

15

3

White tufted ear marmoset

43

10 55

3.2

86.0

3.6

2.7

7.4

19

6

Aye aye

4

25 85

4.1

83.5

5.8

3.9

6.1

21

DUPC

Verreaux's Sifaka

3

62 97

7.2

73.4

12.6

6.8

4.8

22

DUPC

Proboscidea

African elephant

6

60 80

3.7

82.7

5.0

4.0

5.3

24

2

Rodentia

Naked mole rat

5

8 12

3.7

84.1

4.8

4.5

5.1

28

NZP

Guinea pig

17

3 13

4.8

81.2

6.3

6.13

5.6

30

2

House mouse

5

9 10

13.7

59.2

27.0

12.5

2.6

22

3

aFor scientific binomials, see Ref. 4 and for data on additional species, see Refs. 2 and 3. bEnergy calculated as in Ref. 2. cProtein is total nitrogen x 6.38.

Entries without a numbered source reference are unpublished data for milk samples obtained from: BU Beijing University, Beijing, China; CZS Chicago Zoological Society, Chicago, IL; DUPC Duke University Primate Center, Durham, NC; DZ Dallas Zoo, Dallas, TX; DZG Denver Zoological Gardens, Denver, CO; MCZG Milwaukee County Zoological Gardens, Milwaukee, WI; NZP National Zoological Park, Washington, DC. Analytic methods: water by oven drying, fat by Roese Gottlieb extraction, protein (total nitrogen x 6.38) by Kjeldahl or CHN elemental gas analysis, sugar by phenol sulfuric acid. From Ref. 3. eProtein is protein nitrogen x 6.38.

aFor scientific binomials, see Ref. 4 and for data on additional species, see Refs. 2 and 3. bEnergy calculated as in Ref. 2. cProtein is total nitrogen x 6.38.

Entries without a numbered source reference are unpublished data for milk samples obtained from: BU Beijing University, Beijing, China; CZS Chicago Zoological Society, Chicago, IL; DUPC Duke University Primate Center, Durham, NC; DZ Dallas Zoo, Dallas, TX; DZG Denver Zoological Gardens, Denver, CO; MCZG Milwaukee County Zoological Gardens, Milwaukee, WI; NZP National Zoological Park, Washington, DC. Analytic methods: water by oven drying, fat by Roese Gottlieb extraction, protein (total nitrogen x 6.38) by Kjeldahl or CHN elemental gas analysis, sugar by phenol sulfuric acid. From Ref. 3. eProtein is protein nitrogen x 6.38.

monotremes, marsupials, primates, carnivores, and other mammals.[8] At midlactation the total sugar content of milk ranges from about 0.2% to 9% in eutherian mammals (Table 2), and from 6% to 14% in marsupials.[3]

Lactose is synthesized only by mammary epithelial cells, and occurs nowhere else in nature. The biochemical pathways by which lactose is synthesized, and how these may have evolved, have been much studied and debated. Molecular and genetic evidence suggest that the constituents of lactose synthetase may have an ancient origin, predating the appearance of mammals by 100 million years or more.

In suckling young, lactose is digested by an intestinal brush-border enzyme, lactase. It is less clear how and to what extent oligosaccharides are digested. One hypothesis is that oligosaccharides in human milk have antibacterial properties that are most effective if the oligosaccharides survive passage through the intestines.[8] In marsupials, oligosaccharides represent such a large proportion of energy that it is thought they must be digested, perhaps following uptake into intestinal cells by pinocytosis.

OTHER CONSTITUENTS

Species differences occur relative to other nutrients, some of which have practical importance in the feeding of infant mammals. Calcium and phosphorus levels are correlated to milk casein content, but some marine mammals have very low calcium levels and inverse calcium phosphorus ratios. Ruminant milks are so low in iron that suckling young must obtain an environmental source (such as vegetation or dirt) to avoid iron deficiency. By contrast, mammals with very altricial young produce iron-rich milks. The very low vitamin D levels in many primate and ruminant milks may produce vitamin D deficiency if the young are not provided access to ultraviolet B light needed for vitamin D synthesis in skin. In ruminants and horses, milk consumed immediately after birth is a vital source of immunoglobulins that provide passive immunity, but in many other mammals immunoglobulins cross the placenta before birth, so milk immunoglobulins are less crucial. Milk may be an important source of enzymes, growth factors, and hormones, but variation among species is not well studied.

CONCLUSION

Milk is needed by suckling young of all species. The physiologic, digestive, and nutritional consequences of the remarkable differences among mammals in milk composition are only partially understood. Nonetheless, it is sound practice in feeding neonatal mammals to mimic the composition of mother's milk.

ACKNOWLEDGMENTS

I would like to thank collaborators who helped acquire the unpublished data in Table 2, especially Wendy Hood,

Nancy Irlbeck, David Kessler, Prof. Pan, Andy Teare, and Kathy Williams.

ARTICLES OF FURTHER INTEREST

Lactation, Land Mammals, Species Comparisons, p. 562 Lactation, Marine Mammals, Species Comparisons, p. 565

REFERENCES

1. Jenness, R. The Composition of Milk. In Lactation: A Comprehensive Treatise; Larson, B.L., Smith, V.R., Eds.; Academic Press: New York, 1974; Vol. 3, 3 107.

2. Oftedal, O.T. Milk composition, milk yield and energy output at peak lactation: A comparative review. Symp. Zool. Soc. Lond. 1984, 51, 33 85.

3. Oftedal, O.T.; Iverson, S.J. Comparative Analysis of Nonhuman Milks. A. Phylogenetic Variation in the Gross Composition of Milks. In Handbook of Milk Composition; Jensen, R.G., Ed.; Academic Press: San Diego, 1995; 749 789.

4. Wilson, D.E; Cole, F.R. Common Names of Mammals of the World; Smithsonian Institution Press: Washington, DC, 2000.

5. Iverson, S.J.; Oftedal, O.T. Comparative Analysis of Nonhuman Milks. B. Phylogenetic and Ecological Varia tion in the Fatty Acid Composition of Milks. In Handbook of Milk Composition; Jensen, R.G., Ed.; Academic Press: San Diego, 1995; 789 827.

6. Power, M.L.; Oftedal, O.T.; Tardif, S.D. Does the milk of callitrichid monkeys differ from that of larger anthropoids? Am. J. Primatol. 2002, 56, 117 127.

7. Lonnerdal, B.; Atkinson, S. Nitrogenous Components of Milk. A. Human Milk Proteins. In Handbook of Milk Composition; Jensen, R.G., Ed.; Academic Press: San Diego, 1995; 351 368.

8. Urashima, T.; Saito, T.; Nakamura, T.; Messer, M. Oligosaccharides of milk and colostrum of nonhuman mammals. Glycoconjugate J. 2001, 18, 357 371.

9. Hood, W.R.; Kunz, T.H.; Oftedal, O.T.; Iverson, S.J.; LeBlanc, D.; Seyjagat, J. Interspecific and intraspecific variation in proximate, mineral and fatty acid composition of milk in Old World fruit bats (Chiroptera: Pteropodidae). Physiol. Biochem. Zool. 2001, 74, 134 146.

10. Green, B.; Krause, W.J.; Newgrain, K. Milk composition in the North American opossum (Didelphis virginiana). Comp. Biochem. Physiol. 1996, 113B, 619 623.

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