Mayer (1997) presented evidence, based on a

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1 Journal of Horticultural Science & Biotechnology (2005) 80 (6) Historical variation in the mineral composition of edible horticultural products By P. J. WHITE 1 and M. R. BROADLEY 2* 1 Warwick HRI, University of Warwick, Wellesbourne, Warwick CV35 9EF, UK 2 Plant Sciences Division, School of Biosciences, University of Nottingham, Sutton Bonington, Leicestershire, LE12 5RD, UK ( martin.broadley@nottingham.ac.uk) (Accepted 8 July 2005) SUMMARY Historical variation in the mineral composition of edible horticultural products was determined from UK and USA food survey data. From these data, it was possible to measure the variation in the mineral composition of edible horticultural products in general, and in edible horticultural products grouped as vegetables, fruits or nuts, in the 1930s and in the 1980s (or later) for both countries. Thus, the hypothesis that the mineral composition of edible horticultural products had altered since the 1930s was tested. The average concentrations of Cu, Mg and Na in the dry matter of vegetables, and the average concentrations of Cu, Fe and K in fruits decreased significantly between the 1930s and the 1980s in the UK. The same hypothesis was tested with comparable data from the USA, whose historical horticultural and consumer practices have paralleled those of the UK. Data from the USA showed that the average Ca, Cu and Fe concentrations in the dry matter of vegetables, and the average concentrations of Cu, Fe and K in fruits had decreased significantly since the 1930s. There were insufficient data to determine if the mineral composition of any single edible horticultural species had altered significantly over time either in the UK or in the USA. The nutritional implications of this study are discussed. Since horticultural products in general, and fruits and nuts in particular, are relatively small contributors of minerals to the average UK diet, historical changes in mineral composition are unlikely to be significant in overall dietary terms. Mayer (1997) presented evidence, based on a comparison of the data from McCance and Widdowson (1960) and Holland et al. (1991b), which indicated that the average dry matter content and mineral concentrations in fresh vegetables and fruits available in the UK had decreased since the 1930s. Since Mayer s paper, this sentiment has been repeated in the popular press, where the decrease in mineral concentrations in UK vegetables and fruits is often attributed to modern breeding and/or cultural practices. Thus, it is important to ascertain the statistical validity of these claims, since, if they are correct, there are opportunities to improve crop genotypes and cultural practices. Here, we test the hypothesis that the mineral composition of vegetables, fruits and nuts available in the UK has altered since the 1930s. Data were obtained from the original notebooks of McCance and Widdowson ( ) and from the Sixth Summary Edition of McCance and Widdowson s The Composition of Foods (Food Standards Agency, 2002). In contrast to the study by Mayer (1997), mineral concentration data were expressed on a dry weight (DW) basis to remove the variations caused by tissue hydration. Further, the same hypothesis was tested with comparable data from the USA, whose historical horticultural and consumer practices have paralleled those in the UK. Since horticultural products in general, and fruits and nuts in particular, are relatively small contributors of minerals to most UK diets, historical changes in their *Author for correspondence. mineral composition are unlikely to impact significantly on dietary intakes. However, if considered desirable, crop genotypes with higher mineral concentrations could be selected or bred, whilst agronomic interventions based on micro-nutrient fertilisation strategies could also be used to alter crop mineral compositions. MATERIALS AND METHODS Primary data Data on Ca, Cl, Cu, Fe, K, Mg and Na concentrations in horticultural produce available in the UK between were taken from the laboratory notebooks of McCance and Widdowson (Analysis of Foodstuffs, The Wellcome Library for the History and Understanding of Medicine, London. GC/97/A). Data on P concentrations were taken from McCance et al. (1938). These data were compared with the most recent analyses of UK produce, contained in the Sixth Summary Edition of McCance and Widdowson s The Composition of Foods (Food Standards Agency, 2002). However, it should be noted that the data for mineral concentrations in raw vegetables, fruits and nuts in this publication were taken from supplements to the Fourth and Fifth Editions published by Holland et al. (1991a; 1992), which are mostly derived from analyses undertaken between The Ca, Cu, Fe, K, Mg and P concentrations in produce available in the USA in the 1940s were taken from Beeson (1941). These data were compared with values abstracted from the United States Department of Agriculture (USDA) National

2 P. J. WHITE and M. R. BROADLEY 661 Nutrient Database for Standard Reference, Release 16 ( which represent the mineral concentrations in present-day produce. All data were expressed on a DW basis (Tables I and II). Clearly, the data must be interpreted subject to the caveat that analytical techniques have changed and become more sensitive since the 1930s. Statistical analyses The hypothesis that DW-based mineral concentrations in vegetables, fruits and nuts had altered since the 1930s was tested for each mineral element. A new/old quotient was calculated for each crop and mineral element (Table III). The natural logarithm of the new/old quotient was taken and a one sample, twotailed, t-test was performed with the null hypothesis that the logarithm of the quotient was equal to zero (Tables IV and V). A value significantly less than zero indicated a decline in mineral concentration, and a value significantly greater than zero indicated an increase in mineral concentration. Since each comparison was based on independent data for each mineral, no post hoc Type I error corrections were applied. All analyses were performed using GenStat (Release ; VSN International, Oxford, UK). RESULTS The data of McCance and Widdowson ( ), McCance et al. (1938) and Holland et al. (1991a; 1992) were not originally intended to be used to document historical trends in the mineral composition of horticultural produce. Instead, they are representative values of mineral concentrations for different types of produce (Tables I and II). Occasionally, data are given for different varieties of a vegetable or fruit, but this is not common. The sampling procedure for each vegetable, fruit or nut was to purchase a representative sample from several sources and to bulk these together prior to mineral analysis. Multiple analyses of the composite samples were then performed. Unfortunately, this sampling procedure does not allow the biological or genetic variation within a particular crop to be assessed. Without knowledge of this variation, it cannot be determined whether the representative values of mineral concentrations cited for a particular vegetable, fruit or nut differed significantly between the 1930s and the 1980s. Thus, there are insufficient data in these publications to test the hypothesis that the mineral composition of any individual horticultural crop product has declined. However, values for produce in general can be compared between the 1930s and 1980s, and therefore an estimate of variation can be derived for the changes in mineral concentrations in many different crops (Tables IV and V). The new/old quotient for different crops and mineral elements varied considerably, with the concentrations of some minerals in some crops declining, and the concentrations of some minerals in some crops increasing. Statistical analyses indicated that the average concentrations of Cu, Mg and Na in the dry matter of vegetables, and the average concentrations of Cu, Fe and K in the dry matter of fruits available in the UK decreased significantly between the 1930s and the 1980s (Table IV). This is consistent with the observations of Mayer (1997), who undertook an analysis of the mineral concentrations in 20 raw vegetables and 20 fresh fruits. On a fresh, tissue weight basis, reductions in dry matter content and concentrations of Ca, Cu, Mg and Na in raw vegetables and Cu, Fe, K and Mg in fresh fruits available in the UK were noted over this period (Mayer, 1997). Interestingly, although the average Mg concentration in dried fruits available in the UK had decreased, the average Cu concentration in dried fruits had increased, and a significant increase in the average Cu concentration in nuts was also observed (Table IV). The average concentrations of Ca, Cu and Fe in vegetables available in the USA have decreased significantly since the 1930s (Table V). The decline in Cu is consistent with the decline in Cu in vegetables in the UK over the same period. A decline in Ca and Fe in vegetables is also consistent with a recent analysis of USDA data on horticultural products between 1950 and 1999 (Davis et al., 2004). Furthermore, our data indicate that the average concentrations of Cu, Fe and K in fruits available in the USA have decreased significantly since the 1930s (Table V), which is entirely consistent with data for fruits available in the UK (Table IV). A decrease in Fe concentrations in dried fruits available in the USA since the 1930s was also observed (Table V). However, there was no significant difference in mineral concentrations in nuts in the USA since the 1930s. DISCUSSION It can be concluded that the average concentrations of Cu, Mg and Na in the dry matter of vegetables and the average concentrations of Cu, Fe and K in the dry matter of fruits available in the UK have decreased significantly between the 1930s and the 1980s (Table IV). Since the average concentrations of Cu in the dry matter of vegetables, and the average concentrations of Cu, Fe and K in the dry matter of fruits, have also decreased since the 1930s in the USA (Table V), these phenomena might reflect modern agronomic practices. It is noteworthy that modern fertilisers have lower levels of contaminating metals, and that there has been a major reduction in the use of Cu-containing pesticides in conventional agricultural and horticultural production systems since the 1930s. However, historical changes are unlikely to have significant dietary impacts in the UK. In dietary terms, the UK population consumes more Na per head d 1 than the recommended daily intake (Food Standards Agency, 2003), while table salt can be replaced by sodium salt substitutes containing KCl. Thus, any decrease in the K composition of horticultural produce is unlikely to be an important dietary issue. However, decreases in the average concentration of Cu in vegetables, and in the average concentrations of Cu and Fe in fruits, warrant further consideration. In animals, tissue Cu concentrations are under tight homeostatic control. Although Cu is an essential element, it is toxic at high concentrations. The estimated safe and adequate dietary intake of Cu is mg d 1 (Food Standards Agency, 2003). Copper is necessary for the activity of several key enzymes, such as cytochrome c oxidase, amino acid oxidase, superoxide dismutase and monoamine oxidase, and Cu has been implicated in host

3 662 Mineral concentrations in horticultural crops TABLE I Mineral concentrations of UK vegetables, fruits and nuts recorded in the laboratory notebooks of McCance and Widdowson ( ) and published by McCance et al. (1938), or published by the Food Standards Agency (2002) McCance and Widdowson ( ) Food Standards Agency (2002) K Ca Mg Fe Cu Na Cl P K Ca Mg Fe Cu Na Cl P Vegetables Potato (old) Butter bean Haricot bean Lentil Runner bean Pea Aubergine Cabbage (red) Carrot (old) Celery Chicory Cucumber Lettuce Mushroom Mustard and cress Onion Parsnip Pumpkin Radish Spring onion Swede Tomato Turnip Watercress Endive Horseradish Fruits Apples, eating Apples, cooking Apricots Avocado pear Bananas Blackberries Cherries, eating Cherries, cooking Cranberries Currants, black Currants, red Currants, white Custard Apple Damsons Figs Gooseberries, unripe Gooseberries, ripe Grapes Grapefruit Greengages Lemons, whole Loganberries Medlars Melons, cantaloupe Mulberries Nectarines Oranges Passion Fruit Peaches Pears, eating Pineapple Plums, Victoria Dessert Plums, cooking Pomegranate Quinces Raspberries Rhubarb Strawberries Tangerines Watermelon Dried fruits Apricots Currants Dates Figs Peaches Prunes Raisins Sultanas Nuts Almonds Barcelona Brazil Chestnut Hazelnut Coconut (solid) Peanut Walnut All mineral concentrations are quoted in mg 100 g 1 DW.

4 P. J. WHITE and M. R. BROADLEY 663 TABLE II Mineral concentrations of US vegetables, fruits and nuts listed by Beeson (1941) and those available from the USDA 1 Beeson (1941) USDA (2004) K Ca Mg Fe Cu P K Ca Mg Fe Cu P Vegetables Potato Butter (Lima) bean Haricot (Navy) bean Lentil NA NA NA N.A N.A NA NA NA NA N.A N.A NA Pea Aubergine (Eggplant) NA NA NA NA Cabbage Carrot Celery Chicory, witloof NA NA NA N.A N.A NA Cucumber NA Lettuce Mushroom NA NA NA NA Mustard NA N.A Onion Parsnip Pumpkin N.A Radish NA NA NA NA Spring onion NA NA NA N.A N.A NA Swede (Rutabaga) Tomato Turnip Watercress NA NA NA NA Endive NA NA NA 70.0 N.A NA Fruits Apples NA Apricots NA NA NA 4.3 N.A NA Avocado pear NA NA NA 26.4 N.A NA Bananas NA NA NA NA Blackberries NA NA NA NA Cherries, eating NA NA NA NA Cherries, cooking NA NA NA N.A N.A NA Cranberries NA NA NA NA Currants, black NA NA NA N.A 1.70 NA Currants, red NA NA NA N.A N.A NA Currants, white NA NA NA N.A N.A NA NA NA NA N.A N.A NA Custard Apple NA NA NA N.A N.A NA N.A 74 Figs NA NA NA NA Gooseberries NA NA NA NA Grapes NA NA NA NA Grapefruit NA NA NA NA Lemons, whole N.A Melons, cantaloupe NA NA NA N.A N.A NA Mulberries NA NA NA NA Nectarines NA NA NA N.A N.A NA Oranges NA NA NA NA Passionfruit (Granadilla) NA NA NA N.A N.A NA Peaches NA NA NA 14.0 N.A NA Pears NA NA NA NA Pineapple NA NA NA NA Plums NA NA NA NA Pomegranate NA NA NA N.A N.A NA Quinces NA NA NA NA Raspberries NA NA NA NA Rhubarb NA NA NA NA Strawberries NA Tangerines NA NA NA NA Watermelon NA NA NA NA Dried fruits Apricots NA NA NA N.A N.A NA Currants NA NA NA N.A N.A NA Dates NA NA NA NA Figs NA NA NA N.A N.A NA Peaches NA NA NA N.A N.A NA Prunes NA NA NA NA Raisins NA NA NA N.A N.A NA Sultanas NA NA NA N.A N.A NA Nuts Almonds NA NA NA NA Barcelona NA NA NA N.A N.A NA NA NA NA N.A N.A NA Brazil NA NA NA NA Chestnut NA NA NA NA Hazelnut NA NA NA N.A N.A NA Coconut (solid) NA NA NA N.A 1.10 NA Peanut NA NA NA NA Walnut NA NA NA 3.7 NA NA USDA National Nutrient Database for Standard Reference, Release 16, May All mineral concentrations are quoted in mg 100 g 1 DW.

5 664 Mineral concentrations in horticultural crops TABLE III Quotients of mineral concentrations in the dry matter of vegetables, fruits and nuts available in the UK (1980s/1930s) and in the USA (2004/1930s) calculated from the data presented in Tables I and II UK quotient 1980s/1930s US quotient 2004/1930s K Ca Mg Fe Cu Na Cl P K Ca Mg Fe Cu P Vegetables Potato Butter bean Haricot bean Lentil Runner bean Pea Aubergine (Eggplant) Cabbage Carrot Celery Chicory Cucumber Lettuce Mushroom Mustard and cress Onion Parsnip Pumpkin Radish Spring onion Swede (Rutabaga) Tomato Turnip Watercress Endive Horseradish Fruits Apples, eating Apples, cooking Apricots Avocado pear Bananas Blackberries Cherries, eating Cranberries Currants, black Currants, red Currants, white Custard Apple Damsons Figs Gooseberries, unripe Gooseberries, ripe Grapes Grapefruit Greengages Lemons, whole Loganberries Medlars Melons, cantaloupe Mulberries Nectarines Oranges Passion Fruit (Granadilla) Peaches Pears Pineapple Plums, Victoria Dessert Plums, cooking Quinces Raspberries Rhubarb Strawberries Tangerines Watermelon Dried fruits Apricots Currants Dates Figs Peaches Prunes Raisins Sultanas Nuts Almonds Barcelona Brazil Chestnut Hazelnut Coconut (solid) Peanut Walnut

6 P. J. WHITE and M. R. BROADLEY 665 TABLE IV Statistical analysis to test if the concentrations of Ca, Cl, Cu, Fe, K, Mg, Na and P have declined in UK produce between the 1930s and the 1980s Null hypothesis: log e of 1980s/1930s quotient equals zero Mean quotient Lower Upper Test Mineral n (1980s/1930s) Variance S.D. 1 S.E. 2 95% C.I. 3 95% C.I. statistic (t) d.f. 4 P ALL SAMPLES Ca Cl Cu < declined Fe declined K declined Mg declined Na declined P VEGETABLES a Ca Cl Cu < 0.00 declined Fe K Mg declined Na declined P FRUITS a Ca Cl Cu declined Fe declined K declined Mg Na P DRY FRUITS a Ca Cl Cu increased Fe K Mg declined Na P NUTS a Ca Cl Cu increased Fe K Mg Na P a Pooled values for various appropriate crops listed in Tables I III. 1 S.D. = standard deviation. 2 S.E. = standard error of mean. 3 C.I. = confidence interval. 4 d.f. = degrees of freedom. cell defence mechanisms, red and white blood cell maturation, Fe transport, cholesterol and glucose metabolism, myocardial contractility, bone strength and brain development (Food Standards Agency, 2003). The Food Standards Agency Expert Group on Vitamins and Minerals concluded that Cu deficiency would be rare in the UK (Food Standards Agency, 2003), although it may occur in individuals with a genetic defect, such as Menke s syndrome. Nevertheless, there is considerable genetic variation in the ability of plant species (Broadley et al., 2001) and cultivars to accumulate Cu. For example, Cu concentrations in spinach (Römer and Keller, 2002) and onion (Alvarez et al., 2003) shoots differed by 50% between cultivars; and tubers of different potato cultivars varied over four-fold when grown under comparable conditions (Rivero et al., 2003). Copper concentrations in apples (Iwane, 1991) and strawberries (Hakala et al., 2003) differed by twofold between cultivars, and five cranberry fruit cultivars varied up to 16-fold in their Cu concentrations (Davenport and Provost, 1994). Thus, there may be potential for genetic improvement in the Cu composition of crops. Furthermore, Cu concentrations in vegetables and fruits can be increased by fertilisation (Smilde et al., 1981; Sterrett et al., 1983; Karam et al., 1998; Shuman, 1998; Tüzen et al., 1998; Rengel et al., 1999; Bunzl et al., 2001; Tamoutsidis et al., 2002; Wen et al., 2002; Bolan et al., 2003). However, the combination of crop variety and Cu fertilisation must be managed appropriately to ensure a balance between adequate and excessive Cu nutrition. Animals also require Fe to maintain the activities of many important enzymes, and for vital haem proteins such as haemoglobin, myoglobin and the cytochromes which are involved in oxygen transport and energy metabolism, respectively. Like Cu, Fe is under tight homeostatic control, although unlike Cu, Fe deficiency is common in both industrialised and developing countries (Frossard et al., 2000; Welch and Graham, 2004). The estimated Fe requirement for the UK population is 6 12 mg d 1 (Food Standards Agency, 2003). In the UK, some groups may not receive sufficient amounts of Fe in their diets, in particular bioavailable haem-fe from animal sources, which is more easily absorbed by the gut

7 666 Mineral concentrations in horticultural crops TABLE V Statistical analysis to test if the concentrations of Ca, Cl, Cu, Fe, K, Mg, Na and P have declined in US produce between the 1930s and 2004 Null hypothesis: log e of 2004/1930s quotient equals zero Mean quotient Lower Upper Test Mineral n (2004/1930s) Variance S.D. 1 S.E. 2 95% C.I. 3 95% C.I. statistic (t) d.f. 4 P ALL SAMPLES Ca < declined Cu < declined Fe < declined K Mg P VEGETABLES Ca < declined Cu declined Fe < declined K Mg P FRUITS Ca Cu declined Fe < declined K declined P DRY FRUITS Fe declined Cu NUTS Fe Cu a Pooled values for various appropriate crops listed in Tables II. 1 S.D. = standard deviation. 2 S.E. = standard error of mean. 3 C.I. = confidence interval. 4 d.f. = degrees of freedom. than the tightly-bound non-haem Fe which occurs in plant-derived products. For example, the 2003 UK National Diet and Nutrition Survey estimated that 25% of women had inadequate Fe consumption, rising to > 40% in the year-old age range (Henderson et al., 2003; Marriott and Buttriss, 2003). Notably, total Fe intake does not equate to the Fe status of an individual and Fe-homeostasis is critically dependent on whether an individual is susceptible to blood loss or has a diet low in haem-fe or vitamin C (Food Standards Agency, 2003). The main sources of dietary Fe in the UK are cereals and cereal products (44%), while meat and meat products (17%) and vegetables excluding potatoes (10%) are also significant sources. Fruits and nuts are not significant sources of Fe intake, contributing only 3% of the Fe, and 7% of the K to the average UK diet (Henderson et al., 2003). Thus, any decline in Fe in fruits or nuts will have little impact on the UK diet. To address potential Fe-deficiencies in the UK, there is mandatory fortification of white and brown flour, and many breakfast cereals are fortified with Fe on a voluntary basis (Food Standards Agency, 2003). However, there is considerable genetic variation in the ability of plants to accumulate Fe, and international endeavours to breed staple crops with increased Fe content are being adopted to address Fe-deficiency in the Developing World (Frossard et al., 2000; Welch and Graham, 2004). For example, a 2.6-fold variation in Fe concentrations in field grown Phaseolus genotypes has been the target for a breeding programme at the Centro Internacional de Agricultura Tropical (Welch and Graham, 2004). Iron concentrations in apples (Iwane, 1991) and strawberries (Hakala et al., 2003) differ by only 20 60% between cultivars; however, an eight-fold variation in Fe concentrations has been observed across 11 plum varieties (Nergiz and Yildiz, 1997), and the five cranberry fruit cultivars quoted above differed by almost 20-fold in their Fe concentrations (Davenport and Provost, 1994). Iron concentrations in vegetables and fruits can also be increased by appropriate fertilisation (Shuman, 1998; Rengel et al., 1999; Frossard et al., 2000). In conclusion, the average concentrations of some minerals within a range of horticultural products, in general, has decreased since the 1930s in the UK. Parallel changes can be seen in the USA. However, this phenomenon is unlikely to affect UK diets since the proportion of these minerals derived from horticultural products is generally low (Henderson et al., 2003). If necessary, micro-nutrient fertilisation strategies could be adopted to alter crop mineral composition. However, there is considerable genetic variation between horticultural crop genotypes, and crop selection or breeding could also be used to increase dietary mineral intakes in certain sections of the population in the future. This research was funded by the UK Department for Environment, Food and Rural Affairs (Defra). We thank Brian Smith for stimulating our initial interest in historical trends in mineral composition of edible horticultural products, Ms. Helen Wakely, at the Wellcome Library for the History and Understanding of Medicine for sourcing the laboratory notebooks of McCance and Widdowson, and Mark Roe (Institute of Food Research, Norwich) and Clive Rahn (Warwick HRI) for their comments on sampling and analytical procedures and copper fertilisation, respectively.

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