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Has an aquatic diet been necessary for hominin brain evolution and functional development?

Published online by Cambridge University Press:  08 March 2007

John H. Langdon
John H. Langdon*
Affiliation:
Departments of Biology and Anthropology, University of Indianapolis, 1400 East Hanna Avenue, Indianapolis, IN 46227, USA
*
*Corresponding author: DR John H. Langdon, fax +1 317 788 3546, email [email protected]
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Abstract

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A number of authors have argued that only an aquatic-based diet can provide the necessary quantity of DHA to support the human brain, and that a switch to such a diet early in hominin evolution was critical to human brain evolution. This paper identifies the premises behind this hypothesis and critiques them on the basis of clinical literature. Both tissue levels and certain functions of the developing infant brain are sensitive to extreme variations in the supply of DHA in artificial feeding, and it can be shown that levels in human milk reflect maternal diet. However, both the maternal and infant bodies have mechanisms to store and buffer the supply of DHA, so that functional deficits are generally resolved without compensatory diets. There is no evidence that human diets based on terrestrial food chains with traditional nursing practices fail to provide adequate levels of DHA or othern-3 fatty acids. Consequently, the hypothesis that DHA has been a limiting resource in human brain evolution must be considered to be unsupported.

Keywords

Brain evolutionBrain developmentDHAFatty acidsNutrition
Type
Review Article
Information
British Journal of Nutrition , Volume 96 , Issue 1 , January 2006 , pp. 7 - 17
Copyright
Copyright © The Nutrition Society 2006

References

Anderson, GJ, Neuringer, M, Lin, DS & Connor, WECan prenatal n-3 fatty acid deficiency be completely reversed after birth? Effects on retinal and brain biochemistry and visual function in rhesus monkeys. Pediatr Res (2005) 58 865–872CrossRefGoogle ScholarPubMed
Auestad, N, Scott, DT, Janowsky, JS et al. Visual, cognitive, and language assessments at 39 months: a follow-up study of children fed formulas containing long-chain polyunsaturated fatty acids to 1 year of age. Pediatrics (2003) 112 Pt 1, e177–e183CrossRefGoogle ScholarPubMed
Bakker, EC, Ghys, AJA, Kester, ADM, Vles, JSH, Dubas, JS, Blanco, CE, Hornstra, GLong chain polyunsaturated fatty acids at birth and cognitive function at 7y of age. Eur J Clin Nutr (2003) 57 89–95CrossRefGoogle ScholarPubMed
Ballabriga, AEssential fatty acids and human tissue composition. An overview. Acta Paediatr Suppl (1994) 402 63–68CrossRefGoogle ScholarPubMed
Balter, V, Person, A, Labourdette, N, Drucker, C, Fox, M & Vandermeersch, BLes Néandertaliens étaient-ils essentiellement carnivores? Résultats préliminaires sur les teneurs en Sr et en Ba de la paléobiocénose mammalienne de Saint-Césaire (Arc Neandertals fundamentally carnivores? Preliminary results from Sr and Ba content of the mammalian paleofauna from Saint-Césaire). C R Acad Sci IIa (2001) 332 59–65Google Scholar
Beijers, RJ & Schaafsma, ALong-chain polyunsaturated fatty acid content in Dutch preterm breast milk: differences in the concentrations of docosahexaenoic acid and arachidonic acid due to length of gestation. Early Hum Dev (1996) 44 215–223CrossRefGoogle ScholarPubMed
Bezard, J, Blond, JP, Bernard, A & Clouet, PThe metabolism and availability of essential fatty acids in animal and human tissues. Reprod Nutr Dev (1994) 34 539–568CrossRefGoogle Scholar
Birch, EE, Hoffman, DR, Uauy, R, Birch, DG & Prestidge, CVisual acuity and the essentiality of docosahexaenoic acid and arachidonic acid in the diet of term infants. Pediatr Res (1998) 44 201–209CrossRefGoogle ScholarPubMed
Blumenschine, RJHominid carnivory and foraging strategies and the socio-economic function of early archaeological sites. Phil Trans R Soc Lond B (1991) 334 211–221Google ScholarPubMed
Bocherens, H, Billiou, D, Mariotti, A, Toussaint, M, Patou-Mathis, M, Bonjean, D & Otte, MNew isotopic evidence for dietary habits of Neandertals from Belgium. J Hum Evol (2001) 40 497–505CrossRefGoogle ScholarPubMed
Bocherens, H, Drucker, D, Billiou, D, Patou-Mathis, M & Vandermeersch, BIsotopic evidence for diet and subsistence pattern of the Saint-Césaire I Neanderthal, review and use of a multi-source mixing model. J Hum Evol (2005) 49 71–87CrossRefGoogle ScholarPubMed
Bocherens, H, Fizet, M, Mariotti, A, Lange-Badre, B, Vandermeersch, B, Borel, JP & Bellon, GIsotopic biogeochemistry (13C, 15N)of fossil vertebrate collagen: application to the study of a past food web including Neandertal man. J Hum Evol (1991) 20 481–492CrossRefGoogle Scholar
Boris, J, Jensen, B, Salvig, JD, Secher, NJ & Olsen, SFA randomized controlled trial of the effect of fish oil supplementation in late pregnancy and early lactation on the n-3 fatty acid content in human breast milk. Lipids (2004) 39 1191–1196CrossRefGoogle ScholarPubMed
Bourre, JMEssential fatty acids and brain development and function. In Essential Fatty Acids and Infant Nutrition, Ghisolfi, J and Putet, GMontrouge, FranceJohn Libby Eurotext (1992) 11–22Google Scholar
Bourre, JM, Francois, M, Youyou, A, Dumont, O, Piciotti, M, Pascal, G & Durand, GThe effects of dietary alpha-linolenic acid on the composition of nerve membranes, enzymatic activity, amplitude of electrophysiological parameters, resistance to poisons and performance of learning tasks in rats. J Nutr (1989) 119 1880–1892CrossRefGoogle ScholarPubMed
Broadhurst, CL, Cunnane, SC & Crawford, MARift Valley lake fish and shellfish provided brain-specific nutrition for early Homo. Br J Nutr (1998) 79 3–21CrossRefGoogle ScholarPubMed
Broadhurst, CL, Wang, Y, Crawford, MA, Cunnane, SC, Parkington, JE & Schmidt, WFBrain-specific lipids from marine, lacustrine, or terrestrial food resources: potential impact on early African Homo sapiens. Comp. Biochem Physiol B (2002) 131 653–673CrossRefGoogle ScholarPubMed
Bunn, HTHunting, power scavenging, and butchering by Hadza foragers and by Plio-Pleistocene Homo.InMeat-Eating and Human Evolution, pp.199–218 [Stanford, CBandBunn, HTeditors]. Oxford: Oxford University Press. 2001Google Scholar
Burdge, GC, Jones, AE&Wootton, SAEicosapentaenoic and docosapentaenoic acids are the principal products of alpha-linolenic acid metabolism in young men. Br J Nutr (2002) 88, 355–363.CrossRefGoogle ScholarPubMed
Burdge, GC&Wootton, SAConversion of a-linolenic acid to eicosapentaenoic and docosahexaenoic acids in young women. Br J Nutr (2002) 88, 411–420.CrossRefGoogle Scholar
Carlson, SEDocosahexaenoic acid and arachidonic acid in infant development. Semin Neonatol (2001) 6, 437–449.CrossRefGoogle ScholarPubMed
Carlson, SE, Werkman, SH, Rhodes, PG & Tolley, EAVisualacuity development in healthy preterm infants: effect of marineoil supplementation. Am J Clin Nutr (1993) 58, 35–42.CrossRefGoogle ScholarPubMed
Carlson, SE, Werkman, SH&Tolley, EAffect of long-chain n-3 fatty acid supplementation on visual acuity and growth of preterm infants with and without bronchopulmonary dysplasia. E. Am J Clin Nutr. 1996 63, 687–697.CrossRefGoogle Scholar
Carnielli, VP, Darcos, JL, Wattimena, IH, Luijendijk, AB, Herman, JD&Pieter, JJSThe very low birth weight premature infant is capable of synthesizing arachidonic and docosahexaenoic acids from linoleic and linolenic acids. Pediatr Res (1996) 40, 169–174.CrossRefGoogle ScholarPubMed
Chamberlain, JG, & The possible role of long-chain, omega-3 fatty acids in human brain phylogeny. Perspect Biol Med (1996) 39, 436–445.CrossRefGoogle ScholarPubMed
Chulei, R, Xiaofang, L, Hongsheng, M, Xiulan, M, Guizheng, L, Gianhong, D, DeFrancesco, CA&Connor, WEMilk composition in women from five different regions of China: the great diversity of milk fatty acids. J Nutr (1995) 125, 2993–2998.CrossRefGoogle Scholar
Clandinin, MTBrain development and assessing the supply of polyunsaturated fatty acid. Lipids (1999) 34, 131–137.CrossRefGoogle ScholarPubMed
Clandinin, MT, Chappell, JE, Heim, T, Swyer, PR&Chance, GWFatty acid utilization in perinatal de novo synthesis of tissues. Early Hum Dev (1981) 5, 355–366.CrossRefGoogle ScholarPubMed
Connor, WE&Neuringer, MThe effects of n-3 fatty acid deficiency and repletion upon the fatty acid composition and function of the brain and retina. Prog Clin Biol Res (1988) 282, 275–294.Google ScholarPubMed
Cordain, L, Miller, LB, Eaton, SB, Mann, N, Holt, SHA&Speth, JDPlant-animal subsistence ratios and macronutrient energy estimations in worldwide hunter-gatherer diets. Am J Clin Nutr (2000) 71, 682–692.CrossRefGoogle ScholarPubMed
Cordain, L, Watkins, BA&Mann, NJFatty acid composition and energy density of foods available to African hominids: evolutionary implications for human brain development. World Rev Nutr Diet (2001) 90, 144–161.CrossRefGoogle ScholarPubMed
Crawford, MAThe role of dietary fatty acids in biology: their place in the evolution of the human brain. Nutr Rev (1992) 50, 3–11.CrossRefGoogle ScholarPubMed
Crawford, MA, & Placental delivery of arachidonic and docosahexaenoic acids: implications for the lipid nutrition of preterm infants. Am J Clin Nutr (2000) 71, Suppl., 275S–284S.CrossRefGoogle ScholarPubMed
Crawford, MACerebral evolution. Nutr Health (2002) 16, 29–34.CrossRefGoogle ScholarPubMed
Crawford, MA, Casperd, NM&Sinclair, AJThe long chain metabolites of linoleic and linolenic acids in liver and brain in herbivores and carnivores. Comp Biochem Physiol ((1976a)) B54, 395–401.Google Scholar
Crawford, MA, Hassam, AG&Williams, GEssential fatty acids and fetal brain growth. Lancet i (1976b) 452–453.CrossRefGoogle Scholar
Cunnane, S, & Modelling human infant requirements for longchain polyunsaturated fatty acids. Br J Nutr (1999) 82, 163–164.CrossRefGoogle ScholarPubMed
Cunnane, SC, Harbige, LS&Crawford, MAThe importance of energy and nutrition supply in human brain nutrition. Nutr Health (1993) 9, 219–235.CrossRefGoogle Scholar
De Groot, RH, Hornstra, G, van Houwelingen, AC&Roumen, FEffect of alpha linolenic acid supplementation during pregnancy on maternal and neonatal polyunsaturated fatty acid status and pregnancy outcome. Am J Clin Nutr (2004) 79, 251–260.CrossRefGoogle ScholarPubMed
de Heinzelin, J, Clark, JD, White, T, Hart, W, Renne, P, Woldegabriel, G, Beyene, Y&Vrba, EEnvironment and behavior of 2.5-million-year-old Bouri hominids. Science 284, (1999) 625–629.CrossRefGoogle ScholarPubMed
De Vriese, SR, Matthys, C, De Henauw, S, De Backer, G, Dhont, M&Christophe, ABMaternal and umbilical fatty acid status in relation to maternal diet. Prostaglandins Leukot Essent Fatty Acids (2002) 67, 389–396.CrossRefGoogle ScholarPubMed
Dorozynski, A&Anderson, ACollagen: a new probe into prehistoric diet. Science (1991) 254, 520–521.CrossRefGoogle ScholarPubMed
Eaton, SBHumans, lipids, and evolution. Lipids (1992) 27, 814–820.CrossRefGoogle ScholarPubMed
Eaton, SB & Konner, MPaleolithic nutrition: a consideration of its nature and current implications. New Engl J Med (1985) 312, 283–289.CrossRefGoogle ScholarPubMed
Ellison, PTHuman ovarian function and reproductive ecology: new hypotheses. Am Anthropol (1990) 92, 933–952.CrossRefGoogle Scholar
Farquharson, J, Cockburn, F, Patrick, WA, Jamieson, EC&Logan, RWInfant cerebral cortex phospholipid fatty-acid composition and diet. Lancet (1992) 340, 810–813.CrossRefGoogle ScholarPubMed
Francois, CA, Connor, SL, Bolewicz, LC&Connor, WESupplementing lactating women with flaxseed oil does not increase docosahexaenoic acid in their milk. Am J Clin Nutr (2003) 77, 226–233.CrossRefGoogle Scholar
Friedman, ZEssential fatty acid requirements for term and preterm infants.InLipids in Modern Nutrition, pp.79– 92 [Horisberger, M and Bracco, U editors]. New York: Raven Press. 1987Google Scholar
Frisch, REFemale Fertility and the Body Fat Connection. Chicago: University of Chicago Press. (2002)Google Scholar
Garcia-Calatayud, S, Redondo, C, Martín, E, Ruiz, JI, García-Fuentes, M&Sanjuro, PBrain docosahexaenoic acid status and learning in young rats submitted to dietary long-chain polyunsaturated fatty acid deficiency and supplementation limited to lactation. Pediatr Res (2005) 57, 719–723.CrossRefGoogle ScholarPubMed
Gerster, HCan adults adequately convert a-linolenic acid (18:3n-3) to eicosapentaenoic acid (20:5n-3) and docosahexaenoic acid (22:6n-3)?. Int J Vitam Nutr Res (1997) 68, 159–173.Google Scholar
Ghys, A, Bakker, E, Hornstra, G&van den Hout, MRed blood cell and plasma phospholipid arachidonic and docosahexaenoic acid levels at birth and cognitive development at 4 years of age. Early Hum Dev (2002) 69, 83–90.CrossRefGoogle ScholarPubMed
Gibson, RA & Kneebone, GMFatty acid composition of human colostrum and mature breast milk. Am J Clin Nutr (1981) 34, 252–257.CrossRefGoogle ScholarPubMed
Gibson, RA & Makrides, MThe role of long chain polyunsaturated fatty acids (LCPUFA) in neonatal nutrition. Acta Paediatr (1998) 87, 1017–1022.Google ScholarPubMed
Gibson, RA & Makrides, Mn-3 Polyunsaturated fatty acid requirements of term infants. Am J Clin Nutr (2000) 71, Suppl., 251S–255S.CrossRefGoogle ScholarPubMed
Gibson, RA & Rassias, G (1990) Infant nutrition and human milk. In Omega-6 Essential Fatty Acids: Pathophysiology and Roles in Clinical Medicine, pp.283–293.[Horrobin, DR, editors]. New York: Alan R Liss.Google Scholar
Gil, A, Ramirez, M&Gil, MRole of long-chain polyunsaturated fatty acids in infant nutrition. Eur J Clin Nutr (2003) 57, Suppl. 1. S31–S34.CrossRefGoogle ScholarPubMed
Giltay, EJ, Gooren, LJ, Toorians, AW, Katan, MB&Zock, PLDocosahexaenoic acid concentrations are higher in women than in men because of estrogenic effects. Am J Clin Nutr (2004) 80, 1167–1174.CrossRefGoogle ScholarPubMed
Grine, FE, Klein, RG&Volman, TPDating, archaeology and human fossils from the Middle Stone Age levels of Die Kelders, South Africa. J Hum Evol (1991) 21, 363–395.CrossRefGoogle Scholar
Guesry, PThe role of nutrition in brain development. Prev Med (1998) 27, 189–194.CrossRefGoogle ScholarPubMed
Haenel, HPhylogenesis and nutrition. Die Nahrung (1989) 33, 867–887.Google ScholarPubMed
Haggarty, PEffect of placental function on fatty acid requirements during pregnancy. Eur J Clin Nutr (2004) 58, 1559–1570.CrossRefGoogle ScholarPubMed
Helland, IB, Smith, L, Saarem, K, Saugstad, OD & Drevon, CAMaternal supplementation with very-long-chain n-3 fatty acids during pregnancy and lactation augments children's IQ at 4 years of age. Pediatrics (2003) 111, e39–e44.CrossRefGoogle ScholarPubMed
Hoberg, EP, Alkire, NL, de Queiroz, A&Jones, AOut of Africa: origins of the Taenia tapeworms in humans. Proc R Soc Lond B Biol Sci (2000) 268, 781–787.CrossRefGoogle Scholar
Hoffman, DR, Birch, EE, Castañ;eda, YS, Fawcett, SL, Wheaton, DS, Birch, DG&Uauy, RVisual function in breast-fed term infants weaned to formula with or without long-chain polyunsaturates at 4 to 6 months: a randomized clinical trial. J Pediatr (2003) 142, 669–677.CrossRefGoogle ScholarPubMed
Hoffman, DR, Theuer, RC, Castañeda, YS, Wheaton, DH, Bosworth, RG, O'Connor, AR, Morale, SE, Wiedemann, LE&Birch, EEMaturation of visual acuity is accelerated in breast-fed term infants fed baby food containing DHA-enriched egg yolk. J Nutr (2004) 134, 2307–2313.CrossRefGoogle ScholarPubMed
Innis, SM, & Plasma and red blood cell fatty acid values as indexes of essential fatty acids in the developing organs of infants fed with milk or formulas. J Pediatr (1992) 120, 4 Pt 2, S78–S86.CrossRefGoogle ScholarPubMed
Innis, SMFatty acid requirements of the newborn. Can J Physiol Pharmacol (1994) 72, 1483–1492.CrossRefGoogle ScholarPubMed
Innis, SMEssential fatty acids in infant nutrition: lessons and limitations from animal studies in relation to studies on infant fatty acid requirements. Am J Clin Nutr (2000) 71, Suppl., 238S–244S.CrossRefGoogle ScholarPubMed
Innis, SMPerinatal biochemistry and physiology of long-chain polyunsaturated fatty acids. J Pediatr (2003) 143, Suppl.4, S1–S8.CrossRefGoogle ScholarPubMed
Innis, SM, Nelson, CM, Lwanga, D, Rioux, FM&Waslen, PFeeding formula without arachidonic acid and docosahexaenoic acid has no effect on preferential looking acuity of recognition memory in healthy full-term infants at 9 mo of age. Am J Clin Nutr (1996) 64, 40–46.CrossRefGoogle ScholarPubMed
Jensen, CL & Heird, WCLipids with an emphasis on longchain polyunsaturated fatty acids. Clin Perinatol. 2002 29, 261–281.CrossRefGoogle ScholarPubMed
Jensen, CL, Maude, M, Anderson, RE&Heird, WCEffect of docosahexaenoic acid supplementation of lactating women on the fatty acid composition of breast milk lipids and maternal and infant plasma phospholipids. Am J Clin Nutr (2000) 71, Suppl., 292S–299S.CrossRefGoogle ScholarPubMed
Jones, FA, & New concepts in human nutrition in the twentieth:the special role of micro-nutrients century. J Nutr Med (1994) 4, 99–114.Google Scholar
Jorgensen, MH, Holmer, G, Lund, P, Hernell, O&Michaelsen, KFEffect of formula supplemented with docosahexaenoic acid and gamma-linolenic acid on fatty acid status and visual acuity in term infants. J Pediatr Gastroenterol Nutr (1998) 26, 412–421.Google Scholar
Kelly, RLThe Foraging Spectrum: Diversity in Hunter-Gatherer Lifeways. Washington: Smithsonian Institution Press. 1995Google Scholar
Khedr, EMH, Farghaly, WMA, Amry, S-E-D&Osman, AAANeural maturation of breast- and formula-fed infants. Acta Paediatr (2004) 93, 734–798.CrossRefGoogle ScholarPubMed
Klein, RG, & The stone age prehistory of southern Africa. Annu Rev Anthropol (1983) 12, 25–48.CrossRefGoogle Scholar
Klein, RGThe Human Career, 2nd ed, Chicago: University of Chicago Press. 1999Google Scholar
Kohn, GHuman milk and fatty acids: quantitative aspects. InEssential Fatty Acids and Infant Nutrition, pp.79–88 [Ghisolfi, J and Putet, G, editors]. Montrouge, France: John Libby Eurotext. 1992Google Scholar
Koletzko, B, Fats for brains. Eur J Clin Nutr (1992) 46 Suppl 1S51–S62.Google ScholarPubMed
Koletzko, B, Rodríguez-Palermo, M, Demmelmair, H, Fidler, N, Jensen, R, Sauerwald, T, Physiological aspects of human milk lipids. Early Hum Dev (2001) 65 Suppl. S3–S18.CrossRefGoogle ScholarPubMed
Koo, WWK, Efficacy and safety of docosahexaenoic acid and arachidonic acid addition to infant formulas: can one buy better vision and intelligence?. J Am Coll Nutr (2003) 22 101–107.CrossRefGoogle ScholarPubMed
Krasevec, JM, Jones, PJ, Cabrera-Hernandez, A, Mayer, DL, Connor, WE, Maternal and infant essential fatty acid status in Havana, Cuba. Am J Clin Nutr (2002) 76 834–844.CrossRefGoogle ScholarPubMed
Kris-Etherton, PM, Taylor, DS, Yu-Poth, S, Huth, P, Moriority, K, Fishell, V, Hargrove, RL, Zhao, G, Etherton, TD, Polyunsaturated fatty acids in the food chain in the United States. Am J Clin Nutr (2000) 71 Suppl 179S–188S.CrossRefGoogle ScholarPubMed
Kuipers, RK, Fokkema, MR, Smit, EN, van der Meulen, J, Boersma, ER, Muskiet, FAJ, High contents of both docosahexaenoic and arachidonic acids in milk of women consuming fish from Lake Kitangiri (Tanzania): targets for infant formula close to our ancient diet?. Prostaglandins Leukot Essent Fatty Acids (2005) 72 279–288.CrossRefGoogle ScholarPubMed
Lammi-Keefe, CJ, Jensen, RG, Lipids in human milk: a review 2. Composition and fat soluble vitamins. J Pediatr Gastroenterol Nutr (1984) 3 172–198.Google ScholarPubMed
Lamptey, MS, Walker, BL, A possible essential role for dietary linolenic acid in the development of the young rat. J Nutr (1976) 106 86–93.CrossRefGoogle ScholarPubMed
Lanting, CI, Boersma, ER, Lipids in infant nutrition and their impact on later development. Curr Opin Lipidol (1996) 7 43–47.CrossRefGoogle ScholarPubMed
Lauritzen, L, Jørgensen, MH, Hansen, HS, Michaelsen, KF, Fluctuations in human milk long-chain PUFA levels in relation to dietary fish intake. Lipids (2002) 37 237–244.CrossRefGoogle ScholarPubMed
Lauritzen, L, Jørgensen, MH, Mikkelsen, TB, Skovgaard, IM, Staarup, E-M, Olsen, SF, Høy, C-E, Michaelsen, KF, Maternal fish oil supplementation in lactation: effect on visual acuity and n-3 fatty acid content of infant erythrocytes. Lipids (2004) 39 195–206.CrossRefGoogle ScholarPubMed
Lefkowitz, W, Lim, S-Y, Lin, Y, Salem, N, Where does the developing brain obtain its docosahexaenoic acid? Relative contributions of dietary α-linolenic acid, docosahexaenoic acid, and body stores in the developing rat. Pediatr Res (2004) 57 157–165.CrossRefGoogle ScholarPubMed
McBrearty, S, Brooks, ASThe revolution that wasn't: a new interpretation of the origin of modern human behavior. J Hum Evol (2000) 39 453–563.CrossRefGoogle ScholarPubMed
Makrides, M, Neumann, M, Simmer, K, Pater, J, Gibson, R (1995) Are long-chain polyunsaturated fatty acids essential nutrients in infancy?. Lancet 345 1463–1468.CrossRefGoogle ScholarPubMed
Malcolm, CA, Hamilton, R, McCulloch, DL, Montgomery, C, Weaver, LT, Scotopic electroretinogram in term infants born of mothers supplemented with docosahexaenoic acid during pregnancy. Invest Ophthalmol Vis Sci (2003) 44 3685–3691.CrossRefGoogle ScholarPubMed
Mannino, MA, Thomas, KD, Depletion of a resource?The impact of prehistoric human foraging on intertidal mollusc communities and its significance for human settlement, mobility, and dispersal. World Archaeol (2002) 33 452–474.CrossRefGoogle Scholar
Marangoni, F, Agostoni, C, Lammardo, AM, Bonvissuto, M, Giovannini, M, Galli, C, Riva, E, Polyunsaturated fatty acids in maternal plasma and in breast milk. Prostaglandins Leukot Essent Fatty Acids (2002) 66 535–540.CrossRefGoogle ScholarPubMed
Martinez, M, Tissue levels of polyunsaturated fatty acids during early human development. J Pediatr (1992) 120 4 Pt 2 S129–S138.CrossRefGoogle ScholarPubMed
Milton, K, Comparative aspects of diet in Amazonian forestdwellers. Phil Trans R Soc Lond B (1991) 334 253–263.Google ScholarPubMed
Montgomery, C, Speake, BK, Cameron, A, Sattar, N, Weaver, LT, Maternal docosahexaenoic acid supplementation and fetal accretion. Br J Nutr (2003) 90 135–145.CrossRefGoogle ScholarPubMed
Morale, SE, Hoffman, DR, Castañeda, YS, Wheaton, DH, Burns, RA, Birch, EE, Duration of long-chain polyunsaturated fatty acids availability in the diet and visual acuity. Early Hum Dev (2005) 81 197–203.CrossRefGoogle ScholarPubMed
Moriguchi, T, Salem, NRecovery of brain docosahexaenoate leads to recovery of spatial task performance. J Neurochem (2003) 87 297–309.CrossRefGoogle ScholarPubMed
Morris, DH, Methodologic challenges in designing clinical studies to measure differences in the bioequivalence of n-3 fatty acids. Mol Cell Biochem (2003) 246 83–90.CrossRefGoogle ScholarPubMed
Nettleton, JAω-3 fatty acids: comparison of plant and seafood sources in human nutrition J Am Diet Assoc (1991) 91 331–337.CrossRefGoogle ScholarPubMed
Nettleton, JAAre n-3 fatty acids essential nutrients for fetal and infant development?. J Am Diet Assoc (1993) 93 58–64.CrossRefGoogle ScholarPubMed
Neuringer, MCerebral cortex docosahexaenoic acid is lower in formula-fed than in breast fed infants. Nutr Rev (1993) 51 238–241.CrossRefGoogle ScholarPubMed
Neuringer, M, Anderson, GJ & Connor, WEThe essentiality of n-3 fatty acids for the development and function of the retina and brain. Annu Rev Nutr (1988) 8 517–541.CrossRefGoogle ScholarPubMed
O'Dea, KTraditional diet and food preferences of Australian Aboriginal hunter-gatherers. PhilTrans R Soc Lond B (1991) 334 233–241.Google ScholarPubMed
Pawlosky, RJ, Denkins, Y, Ward, G & Salem, NRetinal and brain accretion of long-chain polyunsaturated fatty acids in developing felines: the effects of corn oil-based maternal diets. Am J Clin Nutr 1997 65 465–472.CrossRefGoogle ScholarPubMed
Pawlosky, R, Hibbeln, J, Lin, Y & Salem, Nn-3 Fatty acid metabolism in women. Br J Nutr (2003) 90 993–994.CrossRefGoogle ScholarPubMed
Pitts, MRoberts, MFairweather Eden. NewYork: Fromm International 2000Google Scholar