World Agriculture Vol 5 No 2 by Script Media

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a editorial board

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editors World Agriculture Editorial Board Patrons Professor Yang Bangjie, Member of the Standing Committee of the National People’s Congress of China. (China) Lord Cameron of Dillington, Chair of the UK All Party Parliamentary Group for Agriculture and Food for Development. (UK) Maxwell D. Epstein, Dean Emeritus, International Students and Scholars, University of California, Los Angeles.(USA) Sir Crispin Tickell, GCMG, KCVO, formerly, British Ambassador to the United Nations and the UK’s Permanent Representative on the UN Security Council (UK) Managing Editor and Deputy Chairman Dr David Frape BSc, PhD, PG Dip Agric, CBiol, FRSB, FRCPath, RNutr. Mammalian physiologist Regional Editors in Chief Robert Cook BSc, CBiol, FRSB. (UK) Plant pathologist and agronomist Professor Zhu Ming BS, PhD (China) President of CSAE & President of CAAE Scientist & MOA Consultant for Processing of Agricultural Products & Agricultural Engineering, Chinese Academy of Agricultural Engineering Deputy Editors Dr Ben Aldiss, BSc, PhD, CBiol, MSB, FRES. (UK) Ecologist, entomologist and educationalist Dr Sara Boettiger B.A. ,M.A.,Ph.D (USA) Agricultural economist Professor Neil C. Turner, FTSE, FAIAST, FNAAS (India), BSc, PhD, DSc, (Australia) Crop physiologist, Professor Wei Xiuju BS, MS, PhD (China) Executive Associate Editor in Chief of TCSAE, Soil, irrigation & land rehabilitation engineer Members of the Editorial Board Professor Gehan Amaratunga BSc, PhD, FREng, FRSA, FIET, CEng. (UK & Sri Lanka) Electronic engineer & nanotechnologist Professor Pramod Kumar Aggarwal, B.Sc, M.Sc, Ph.D. (India), Ph.D. (Netherlands), FNAAS (India), FNASc (India) Crop ecologist Dr Andrew G. D. Bean, BSc, PhD, PG Dip. Immunol. (Australia) Veterinary pathologist and immunologist Professor Tim Benton, BA, PhD, FRSB, FLS Food systems, food security, agriculture-environment interactions Professor Phil Brookes BSc, PhD, DSc. (UK) Soil microbial ecologist Professor Andrew Challinor, BSc, PhD. (UK) Agricultural meteorologist Dr Pete Falloon BSc, MSc, PhD (UK) Climate impacts scientist Professor Peter Gregory BSc, PhD, CBiol, FSRB, FRASE. (UK) Soil scientist Professor J. Perry Gustafson, BSc, MS, PhD (USA) Plant geneticist Herb Hammond, (Canada) Ecologist, forester and educator Professor Sir Brian Heap CBE, BSc, MA, PhD, ScD, FRSB, FRSC, FRAgS, FRS (UK) Animal physiologist Professor Fengmin Li, BSc, MSc, PhD, (China) Agroecologist Professor Glen M. MacDonald, BA, MSc, PhD (USA) Geographer Professor Sir John Marsh, CBE, MA, PG Dip Ag Econ, CBiol, FRSB, FRASE, FRAgS (UK) Agricultural economist Professor Ian McConnell, BVMS, MRVS, MA, PhD, FRCPath, FRSE. (UK) Animal immunologist Hamad Abdulla Mohammed Al Mehyas B.Sc., M.Sc. (UAE) Forensic Geneticist Professor Denis J Murphy, BA, DPhil. (UK) Crop biotechnologist Dr Christie Peacock, CBE, BSc, PhD, FRSA, FRAgS, Hon. DSc, FRSB (UK & Kenya) Tropical Agriculturalist Professor R.H. Richards, C.B.E., M.A., Vet. M.B., Ph.D., C.Biol., F.S.B., F.R.S.M., M.R.C.V.S., F.R.Ag.S. (UK) Aquaculturalist Professor John Snape BSc PhD (UK) Crop geneticist Professor Om Parkash Toky, MSc, PhD, FNAAS, (India) Forest Ecologist, Agroforester and Silviculturist Professor Mei Xurong, BS, PhD Director of Scientific Department, CAAS (China) Meteorological scientist Professor Changrong Yan BS, PhD (China) Ecological scientist Advisor to the board Dr John Bingham CBE, FRS, FRASE, ScD (UK) Crop geneticist

Published by Script Media, 47 Church Street, Barnsley, South Yorkshire S70 2AS, UK

WORLD AGRICULTURE

Editorial Assitants Dr. Zhao Aiqin BS, PhD (China) Soil scientist Ms Sofie Aldiss BSc (UK) Rob Coleman BSc MSc (UK) Michael J.C. Crouch BSc, MSc (Res) (UK) Kath Halsall BSc (UK) Dr Wang Liu. BS, PhD (China) Horiculturalist Dr Philip Taylor BSc, MSc, PhD (UK)

Volume 5, Number 2 contents In this issue ... editorials: Weak international institutions prevent the full benefits of science based innovation being secured for consumers or the environment 4-5 Professor Sir John Marsh Good Fats, Obesity, CVD and GM Dr David Frape

scientific: Oils and fatty acids essential for vertebrate health – e.g. fish and Man Dr David Frape

7-14

The supply of fish oil to aquaculture: 15-23 a role for transgenic oilseed crop Dr Richard P Haslam, Dr Sarah Usher, Dr Olga Sayanova, Professor Johnathan A Napier, Dr Monica B Betancor, Professor Douglas R Tocher What is the future for oil palm as a global crop Professor. Denis J. Murphy

24-34

Revised instructions to contributors

35-36

Errata from previous issue

Future papers for Spring Issue 2016: Aquaculture: are the criticisms justified? III – Fish Farming and Atlantic salmon. Professor Dave Little and Dr Jonathan Shepherd Crop landraces: A rediscovered, multifuctional and irreplaceable component of agrobiodiversity. Dr Pinelopi BeBeli et al. Disease resistance and food production Dr Andrew Bean ‘Climate-smart villages – a model to promote synergies between production, adaptation and mitigation in agriculture’ Prof. Pramod Aggarwal et al. Innovative agroforestry for livelihood and environment security in India Dr A.K. Handa, Professor O.P. Toky and Dr S.K. Dhyani

If you wish to submit an article for consideration by the Editorial Board for inclusion in a section of World Agriculture: a) Scientific b) Economic & Social c) Opinion & Comment or d) a Letter to the Editor please follow the Instructions to Contributors printed in this issue and submit by email to the Editor editor@world-agriculture.net ghgh

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editorials

Weak international institutions prevent the full benefits of science based innovation being secured for consumers or the environment Professor Sir John Marsh

Solutions and confrontations

wo of the papers in this edition shed light on assertions commonly made by pressure groups. Murphy, contrary to their claims, shows that expanding plantation palm oil production gives a smaller environmental footprint than traditional small-scale production. Haslam et al., explain the inability of capture fisheries to sustain the level of demand for long chain Omega 3 fatty acids, necessary to meet the nutritional needs of farmed fish of which there is a greatly increased rate of production, demanded by a growing human population. They show that the feed requirements of farmed fish may be satisfied by modified vegetable oils, rather than by depleting stocks of sea fish. In both papers the key technology needed to meet growing demand whilst minimising environmental costs depends upon genetic manipulation. Both papers offer grounds for optimism that, at a time when predicted growth of demand from rising numbers of people and rising income, technology can offer the prospect of reducing further pressures on the natural environment. If production is limited to current technology there are likely to be limitations on sustainable supplies that will require either, some reduction in the numbers of people, or a reduction in per-capita consumption, effectively a reduction in real income. Neither strategy is politically acceptable. Inaction will mean that the burden of adjustment will fall on people who are economically weakest, owing to an inevitable increase in prices as supplies diminish. In contrast these papers show, for two important areas, palm oil and fish oil supplies of â&#x20AC;&#x2DC;omega 3â&#x20AC;&#x2122;, productivity can be substantially increased without irreparable damage to the environment.

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Innovation at this fundamental level means moving into territory that is new. That means facing up to the possibility of unrecognised and damaging side effects for either human health or the environment. If we are to exploit such possibilities we need to abandon the negative philosophy of the precautionary principle and establish a well equipped, broadly based and trusted system of monitoring. This must be the responsibility of government, ideally but probably impracticably, on a global basis. Such a service must command the confidence of the public. In doing so it needs not only to publish its own monitoring reports but also address, and where necessary contest, positions adopted by pressure groups â&#x20AC;&#x201C; one of the functions of World Agriculture. Research and development are not luxuries but necessities, if we are to cope with the challenges that lie ahead. Innovations that increase productivity often emerge from interactions between scientists in their own specialist languages. To discover and apply such productivity-enhancing possibilities needs research to be communicated in language that is understood by policy makers and decision takers. Communication should be a two way process. Scientists need to be aware of what communities want so that they recognise the potential of their new discoveries. World Agriculture provides one route through which this communication can take place.

The importance of a global view A second feature common to these papers is the need to visualise both problems and solutions on a global basis. National boundaries are artificial and political decisions in one location often have unrecognised repercussions on natural processes in distant places.

Production of palm oil, greatly in demand in high and middle-income countries, has expanded dramatically in Indonesia and Malaya bringing changes in wildlife habitat, the decline of traditional communities and exposing the economic stability of both countries to fluctuations in the world price of oil. Similarly, increased success in locating and capturing fish has threatened the sustainability of fish populations and destroyed the livelihoods of traditional fishing communities that have no alternative source of income. Palm oil production is concentrated in S E Asia but its impact on the natural environment may affect the welfare of communities in other continents. Deforestation in order to increase food supplies can have adverse consequences for climate change. The loss of biodiversity, as traditional habitats are destroyed, may not only destroy treasured wild life but deprive the world of genetic resources. The need to control pests and overcome diseases that threaten economically productive farming not only reduces bio-diversity but also may reduce the aesthetic value of landscapes. Success in producing more food is likely to result in increased pressure on natural water supplies. The tensions that result may lead to conflicts between countries dependent on the same natural sources of water. In all these areas we need a regulatory framework that takes a world wide view. Attempts to reach a global consensus on action to regulate the exploitation of natural resources have demonstrated the impotence of international institutions. Governments, faced by environmental problems that are geographically or temporally remote are likely to give greater weight to competing demands from local, wellorganised pressure groups. Retaining power depends on those whose votes will determine their own continuation in office.

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editorials Prestige abroad will not win votes at home. As a result international agreements, and their enforcement, tend to proceed at the rate of the most reluctant. These papers offer prospects for more efficient resource use by employing genetically modified materials. If this is frustrated by restrictions on trade in GM products the result will be avoidable

environmental and economic cost for the world as a whole. Most of the worldâ&#x20AC;&#x2122;s population seek a higher standard of living. But such goals are unattainable if productivity levels do not increase. The rejection of productivity-increasing innovation not only penalises those who are now poor but eventually will impose a decline in living standards on many who are currently affluent.

Such a prospect stresses the importance for global welfare that we learn to use available natural resources more efficiently. The papers by Murphy and Haslam et al. provide an example of how science can contribute to resolve problems in specific product areas to improve efficiency and safeguard natural resources for the world community as a whole.

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editorials

Good Fats, Obesity, CVD and GM David Frape

egetable oils provide more than twice as much net energy per unit weight, compared with proteins or carbohydrates. Fatty foods therefore contribute to obesity in the Western world. Obesity is a contributory factor to the wide occurrence of cardio-vascular disease (CVD) and type 2-diabetes (T2D). Hence, studies to compare the specific effects of fats on CVD replacing carbohydrates must be conducted on the basis of equalizing total energy intake. But surveys of large populations of people to assess the effects of dietary factors, especially fats, on the incidence of CVD, T2D and of cancers, in particular, have the problem of distinguishing the effects of those factors separately from that of body weight, or body mass index. With large amounts of data it is possible to control some of the confounding factors statistically. The evidence from these studies generally points to a relationship between the consumption of saturated fats (fatty acids) and CVD, independent of body weight, or body mass index. Nevertheless, I conclude a major health benefit of the Mediterranean Diet over that of Northern Europe, is not that there is any difference in fat content, but that much of the fat in the former diet is in the form of uncooked oil, whereas that oil in Northern Europe is largely replaced by margarine, for which there is no control by the EU of its trans-fat content (see Frape this Issue pp 7-14). In this Issue we publish two important papers on fats. One, is by Haslam and colleagues, on a polyunsaturated substitute for fish oil in GM-modified false flax (Camelina sativa), that contains high concentrations of two dietary essential highly unsaturated fatty acids. The second is on palm oil, an oil rich in palmitic acid, a saturated fatty acid. Palm oil is derived from the African oil

palm, Elaeis guineensis, the major global vegetable oil crop. Palm oil is consumed daily by over two billion people. Murphy, in this issue, informs us that the production of this oil to meet an ever increasing demand has led to extensive conversion of tropical forests to plantations. In some parts of Southeast Asia, this has had major adverse ecological and environmental consequences, with a reduction in biodiversity, damage to soil and the release of greenhouse gases during the initial clearance of the planting area. These consequences have led to calls for boycotts of products containing palm oil. (A haze is apparent over areas of Malaysia each year caused by burning of natural forest and prohibiting air flights.) But this crop provides an example of the importance of advanced breeding methods, particularly genomics, which are beginning to bear fruit in terms of crop improvement for yield and quality. Without these developments even greater areas of natural forest will be destroyed to keep pace with the demand. Palm oil has the benefit of being relatively stable during storage, owing to its high content of palmitic acid, a fully saturated fatty acid; yet this fatty acid has the disadvantage of its relationship to risk factors of CVD. Olive oil, on the other hand, for which there is a very much lower yield of oil/ha, is rich in oleic acid, a monounsaturated fatty acid, which is considered to be healthy. Palm oil contains only half this amount of oleic acid.(see, Frape, this Issue). The paper by Haslam and colleagues relates to the worldwide shortage of long chain,polyunsaturated omega-3 fatty acids, with five and six double bonds (EPA and DHA) that are considered important in human health. Presently the only significant source of these polyunsaturated omega-3 fatty acids is monocellular oceanic plant

organisms, that are consumed by wild fish, thereby making fish an important source of omega-3 fatty acids for humans. These fatty acids are also critical in the diet of farmed fish. Wild fish stocks are under extreme pressure, owing to over-fishing to meet the increasing demands of a growing world population. Moreover, wild fish are under increasing stress owing to the warming of oceans, which reduces oxygen tension. In order to overcome the scarcity of fish oils rich in these two fatty acids, Haslam et al. at Rothamsted describe the transfer of a group of genes from these oceanic organisms to Camelina sativa, false flax. These genes are needed for the production of EPA and DHA. This plant was chosen as it is a rich source of a-linolenic acid, a C18:3 omega-3 fatty acid, the starting material for the required chain of reactions, and Camelina can be cropped in temperate climates and could become an essential source of EPA and DHA for fish farming as the current source from wild fish oils, becomes increasingly scarce. As noted above, these fatty acids are essential nutrients in the diet of Man and so Camelina would provide an additional and crop-based source. Both these papers define a role for modern genetic manipulation of crops. Without the adoption of GM and other related methods of plant breeding it will be impossible to feed the growing numbers of people, amongst whom, the first to suffer will be those groups that are economically disadvantaged. Moreover, biodiversity will suffer at a faster rate if man does not adopt methods developed and proven by research, and the products of that research are then shown to be safe for human consumption. The reason for this is that even larger areas of our natural landscape will need to be converted to farmland if reliable new research is not adopted in practice.

Errata Vol. 5, No. 1, Falloon et al. 1. Page 36 second column, third paragraph “Figure 9 (from 109)” should be 110, not 109 2. Similarly on p 36 in the figure 9 legend – should be (from 110), not (from 109) 3. Page 28, third column, end of 4th paragraph “wild crop ancestors (27)” should be 37, not 27.

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Oils and fatty acids essential for vertebrate health – e.g. fish and Man Dr David Frape Summary This paper provides explanations both of why essential fatty acids are essential and of biochemical terms which are widely used by the general press. These explanations should aid an appreciation of two of our papers in this issue especially that by Haslam et al. Vegetable oils are extracted mostly from seeds of maize, soyabean, sunflower, linseed, rape, olive, and palm. These oils provide over twice as much net energy/kg compared with starch and so their consumption can contribute to obesity with its adverse effects on health. They are a source of two essential dietary nutrients in the form of the polyunsaturated fatty acids (PUFA), C18:2 6 linoleic acid and C18:3, 3, a-linolenic acid. Olive oil is also a rich source of C18:1, 9, oleic acid, a monounsaturated fatty acid (MUFA), which may contribute to its health benefits. Long chain omega3 fatty acids, C20:5, 3, eicosapentaenoic acid (EPA), and C22:6, 3, docosahexaenoic acid (DHA) are also essential in the diet of vertebrates, but the only major primary source of them is oceanic mono-cellular organisms, phytoplanktons and algae, the foodstuff of oceanic animal life. Thus, production of these oils from a crop which can be grown in temperate climates will be an essential source for fish farming, where their current source from wild fish oils, is becoming scarce. EPA and DHA consumption beneficially influence risk factors of cardio-vascular disease (CVD) when they replace saturated fats in the diet. They are more potent than are a-linolenic acid and linoleic acid, or than oleic acid. All these unsaturated fatty acids are protective against CVD, in comparison to saturated fatty acids, e.g. palmitic acid (C16:0). Nevertheless, palm oil is rich in both palmitic acid and oleic acid (Table 1). Olive oil contains a larger proportion of oleic acid and less palmitic acid than does palm oil, and is considered to be protective. Nevertheless, unsaturated fats are prone to oxidation and rancidity, whereas saturated fats are relatively stable and the hydrogenation of unsaturated vegetable oils during the production of margarine leads to cis—trans isomerisation of unsaturated fats. The trans-isomers have been shown to raise plasma LDL cholesterol levels and to pose a risk for CVD. Hence, legislation has been introduced in the USA, where trans-fat levels must be declared on the labels of appropriate products in the USA. However, compared with the relationship of fatty acids with the risk factors of CVD, the correlation of all these risk factors with the occurrence of CVD is less well secure, for the obvious reason that individuals do not eat nutrients, but mixed diets; so there is confounding of factors on the response to the dietary environment of individuals. Some clarification of this situation is possible in population studies. Key words fats, lipids, risk factors, CVD, GM, definitions Abbreviations CVD, cardiovascular disease; GRAS, generally recognized as safe; MUFA, monounsaturated fatty acids; PUFA, polyunsaturated fatty acids.

Definitions – what are fats? Lipids Lipids are a group of naturally occurring compounds that include fats, waxes, sterols, including cholesterol, fat-soluble vitamins (such as vitamins A, D, E, and K), monoglycerides, diglycerides, triglycerides, phospholipids, and others. The main biological functions of lipids include storing energy, signalling and acting as structural components of cell membranes. Lipids have applications in the cosmetic and food industries as well as in nanotechnology. Although the term lipid is sometimes used as a synonym for fats, fats are a subgroup of lipids called triglycerides or triacylglycerols.

Triglycerides (Triacylglycrols )

Fig. 1 A triglyceride is a compound derived from glycerol and three fatty acid alkyl chains, R1, R11 and R111, forming an ester through their acyl group. These three chains may be identical, or each one may have a different formula.

Triglycerides are the main constituents of vegetable oil (typically containing more unsaturated fatty acids) and animal fats (typically with more saturated fatty acids), see Figure 1 for a typical structure.

Figure 2 shows four different fatty acids. Stearic acid is completely saturated, i.e. it has single bonds (-CH2-CH2-) between the carbon atoms in its chain. Saturated fatty acids are “saturated” with hydrogen – all available places where hydrogen atoms could be bonded to carbon atoms are occupied i.e. each carbon has two H atoms attached to it, whereas the omega (end of the C chain) will have three i.e. a methyl group. Unsaturated compounds have double bonds (-CH=CH-) between carbon atoms, reducing the number of places where hydrogen atoms can bond to carbon atoms to one H atom per C atom, as in oleic acid and in a-linolenic acid (Fig. 2). These carbon bonds are under stress and thus open to oxidation, or to rotation. The fatty acid bonds to the glycerol through its acyl (carboxyl) group in forming a fat. Unsaturated fats have a lower melting point and are more likely to

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scientific C18:1 9

Figure 2 The structural formulae of four fatty acids, the lower two of which are dietary essential fatty acids, in that mammals and fish are incapable of their synthesis from non-essential fatty acids. n.b. The methyl group is at the omega end of the chain, regardless of its length (also known as the n end) and the carboxyl group is at the alpha end.

be liquid at room temperature. Saturated fats have a higher melting point and are more likely to be solid at room temperature. Melting point is also determined by C chain length of the fatty acids shorter chains have a lower melting point. Most natural fats contain a complex mixture of individual triglycerides. Because of this, they melt over a broad range of temperatures. Polyunsaturated fatty acids act as valuable structural components in cell membranes, whereas saturated fats, not used as energy sources, tend to accumulate in the liver, viscera and subcutenaeous fat depots and are a component of arterial plaques.

Fatty acids These are chain-like molecules, the carboxylic acid (-COOH) end of which is considered the beginning of the chain, thus “alpha” with the methyl (CH3) end, as the “tail” of the chain, thus “omega.” Nevertheless, the way in which a fatty acid is named is determined by the location of the first double bond, frequently counted from the methyl end, that is, the omega ( -) or the n- end. The chain lengths of the fatty acids in naturally occurring triglycerides vary, but most contain 16, 18, or 20 carbon atoms. Natural fatty acids found in plants and animals are typically composed of only even numbers of carbon atoms. Bacteria, however, possess the ability to synthesise odd- and branched-chain fatty acids. As a result, ruminant animal fat contains some odd-numbered fatty acids, such as 15, owing to the action

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of bacteria in the rumen. (see Table 1) A short notation is used to define those of each type of fatty acid n.b. see under Transisomers, below, for an explanation of the term “cis”: C18:0 denotes an acid with 18 C atoms in its chain, all of which are saturated with H atoms, a SFA. C18:1, 9 (also known as C18:1n-9), oleic acid, a MUFA, denotes a fatty acid with 18 C atoms in its chain, but it has one unsaturated cis-bond, which is 9 C atoms from the omega ( or n) end, i.e. the methyl-group, of the chain. C18:2, 6 (also C18:2n-6), linoleic acid, a PUFA, denotes a fatty acid with 18 C atoms in its chain, but it has two unsaturated cis-bonds, the first of which is 6 C atoms from the end of the chain, whereas the second double bond is 9 C atoms from the end of the chain. This is a polyunsaturated fatty acid (PUFA). It is one of the essential fatty acids, so called because they are necessary for health, and they cannot be produced adequately within the human body. They must be acquired through diet.). All PUFAs are dietary essential in humans. C20:5, 3 (also C20:5n-3), EPA, a PUFA with 20 C atoms in its chain with five unsaturated cis-bonds, the first of which is 3 C atoms from the end of the chain, whereas the other double bonds are 6, 9, 12 &15 C atoms from the end of the chain. C22:6, 3 (also C22:6N-3), DHA, a PUFA with 22 C atoms in its chain, but with six unsaturated cis-bonds, the first of which is 3 C atoms from the end of the chain, whereas the other double bonds are 6, 9, 12 ,15 & 18 C atoms

from the end of the chain. This is another PUFA. C18:3, 3, a-linolenic acid (ALA), an n-3 PUFA with an 18-carbon chain and three cis double bonds. The first double bond is located at the third carbon from the methyl end of the fatty acid chain, known as the n endthe other two are located at carbons 6 and 9. Thus, a-linolenic acid is a polyunsaturated n-3 (omega-3) fatty acid. ALA is found in seeds: chia, flaxseed, nuts (notably walnuts), and in many common vegetable oils. In terms of its structure, it is also named from the alpha-end as all-cis-9,12,15-octadecatrienoic acid. Its isomer is gamma linoleic acid GLA is 18:3 (n-6). n.b. I used the term cis. It is unfortunately important to understand this term, as legislation is in the process for the declaration of the cistrans composition of fats in food products (see Trans-Isomers, below).

N-3, Omega, 3 Terrestrial plants can be rich in 18C PUFA such as linoleic acid (18:2 6) and a-linolenic acid (ALA, 18:3 3), but the biologically most active omega-3 fatty acids in fish are the long-chain polyunsaturated 3 fatty acids primarily EPA (20 carbons and 5 double bonds) and DHA (22 carbons and 6 double bonds) (Fig. 3). Some freshwater and salmonid species of fish can produce EPA and then from EPA, the more crucial, DHA, but most marine fish are unable to do so in adequate quantities from the shorter-chain omega-3 fatty acid ALA (18 carbons and 3 double bonds) provided in dietary plant sources. The ability of vertebrates to make these longer-chain omega-3 fatty acids from ALA may be impaired even more by aging, and is generally considered not to exceed 5%, so this ability is inadequate to meet their dietary requirement. It may be concluded that vertebrates, including fish, cannot adequately synthesise PUFAs (i.e. fatty acids with more than one double unsaturated bond) because they lack the enzymes required for their production from monounsaturated fatty acids.

Trans-isomers (see Fig. 4) An unwelcome side effect occurs during the partial hydrogenation of the unsaturated fat when some of the cis double bonds are converted into trans double bonds by an isomerization reaction with the catalyst used for the hydrogenation during production to

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Figure 3 The structural formulae of two long chain cis 3 fatty acids (EPA & DHA), essential in the diet of vertebrates, including fish and of Man. The third is a saturated fatty acid rich in palm oil.

raise the melting point of products such as margarine. Cis and trans forms are known as geometric isomers of fatty acids. They are structurally identical except for the arrangement of the double bond, and so the location of the two H atoms in relation to the two carbons is changed. Most natural fatty acids have a cisconfiguration i.e. vegetable sources. The fatty acids in Figs 2 and 3 are all indicated as cis-isomers.

Fig. 4 indicates the change in the bond during trans formation – a structural arrangement possessing a lower energy. There is pressure on legislators to place a legal limit on trans-isomers of unsaturated fatty acids, especially in hydrogenated vegetable fats. In 2013, the United States Food and Drug Administration (FDA) issued a preliminary determination that partially hydrogenated oils (which contain trans fats) are not “generally recognized as safe”. On 16 June 2015, the FDA in the USA set a three-year time limit for their removal from all processed food. Trans fats levels can be reduced or eliminated using saturated fats!1. High intake of trans fatty acids can lead to human health problems as it contributes to obesity, high blood pressure, and a greater risk for heart disease. Trans fat is abundant in fast food restaurants. It is consumed in greater quantities by people who do not have access to a diet consisting of fewer hydrogenated fats, or who often consume fast food2.

Fig. 4 Reaction scheme for three fatty acids in a molecule of a triglyceride (a triacylglycerol): of trans fat during the hydrogenation process for the production of margarine from oils. Up to 45% of the total fat may contain trans fatty acids. The Figure shows a triglyceride containing in one saturated fatty acid, palmitic acid (blue), one mono-unsaturated fatty acid, oleic acid (green), and one polyunsaturated fatty acid, a-linolenic acid, (red). The latter is changed to a trans.oleic acid* (black), the blue remains palmitic acid; whereas the monounsaturated fatty acid (green) becomes saturated stearic acid (black).*see table 1 below for another C18:1 acid, Vaccenic acid.

Health and trans fats There are two accepted blood tests that measure an individual’s risk for coronary heart disease. The first considers ratios of two types of cholesterol, the other the amount of a cellsignalling cytokine called Creactive protein. The ratio test is more accepted, while the cytokine test may be more powerful. The effect of trans fat consumption has been documented3,4,5 . Cholesterol ratio: This ratio compares the levels of LDL to HDL. Trans fat behaves like saturated fat by raising the level of LDL, but, unlike saturated fat, it

has the additional adverse effect of decreasing levels of HDL. The net increase in LDL/HDL ratio with trans fat is approximately double that due to saturated fat. (Higher ratios are worse.). C-reactive protein (CRP): A study of over 700 nurses showed that those in the highest quartile of trans fat consumption had blood levels of CRP that were 73% higher than those in the lowest quartile6,7,8. A 2006 study supported by the National Institutes of Health and the USDA Agricultural Research Service concluded that palm oil is not a safe substitute for partially hydrogenated fats (trans fats) in the food industry, because palm oil results in adverse changes in the blood concentrations of LDL and apolipoprotein B just as trans fat does10,11,12,13,14.

Conjugated Linoleic acid (CLA) Conjugated fatty acids are polyunsaturated fatty acids in which at least one pair of double bonds are separated by only one single bond, as in conjugated linoleic acid, in Fig. 5, whereas in Fig 4 you will notice the three double bonds of alpha-linolenic acid (in red) are separated by one further carbon, i.e. they are not conjugated. Conjugated linoleic acids (CLA) are a family of at least 28 isomers of linoleic acid found mostly in the meat and dairy products derived from ruminants (Table 1). One such isomer of CLA is shown in Fig. 5 CLAs are both a trans and a cis fatty acids. The cis bond causes a lower melting point and ostensibly also the observed beneficial health effects. Unlike other trans fatty acids, they may, therefore, have beneficial effects on human health. In the United States, trans linkages in a conjugated system are not counted as trans fats for the purposes of nutritional regulations and labelling. CLA and some trans isomers of oleic acid are produced by microorganisms in the rumens of ruminants (Table 1).

Fig. 5 Conjugated Linoleic acid which has adjacent trans7- and cis9bonds.

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scientific Non-ruminants, including humans, produce certain isomers of CLA from trans isomers of oleic acid, such as vaccenic acid (not a conjugated fatty acid, as it possesses only one double bond, Table 1), but , which is converted to CLA by the enzyme, delta-9-desaturase. Most studies of CLAs have used a mixture of isomers wherein the isomers c9,t11-CLA (rumenic acid) and t10,c12-CLA were the most abundant. More recent studies using individual isomers indicate that the two isomers have very different health effects15,16. In healthy humans, CLA and the related conjugated linolenic acid (CALA) isomers are bioconverted from linoleic acid and alpha-linolenic acid, respectively, mainly by Bifidobacterium bacteria strains inhabiting the gastrointestinal tract. This bacterium is considered to produce beneficial effects, especially in babies. In 2008, the United States Food and Drug Administration categorized CLA as generally recognized as safe (GRAS). Dietary sources of conjugated linoleic acid Kangaroo meat may have the highest concentration of CLA17. Food products from grass-fed ruminants, e.g. mutton, beef18,dairy products and eggs are good sources of CLA19,20. Some mushrooms, such as Agaricus bisporus and Agaricus subrufescens, are rare non-animal sources of CLA21. Health effects of N-6 and N-3 polyunsaturated fatty acids (i.e. LA, ALA, EPA and DHA ) and monounsaturated fatty acids (e.g. oleic acid) The relationship between blood levels of cholesterol and cardio-vascular disease (CVD), or that between the intake of SFA and PUFA or MUFA and CVD is somewhat inconclusive. Investigations have failed to show an effect on flow-mediated dilatation, or other measures of vascular function; whereas significant beneficial effects on blood lipids and slight beneficial effects on blood pressure have been observed by replacing SFA with either MUFA or PUFA, or by a diet high in carbohydrate 22,23,24,25,26,27. It can be concluded that LC PUFA, (n-6 & n-3) and MUFA do benefit blood lipids when they replace SFA in the diet; but the relationship between this and risk of cardio-vascular disease is less clear. On balance there seems to be a benefit from the use of unsaturated fatty acids. However, it should be borne in mind that margarines, where the melting point of unsaturated oils has been raised, may contain undesirable concentrations of trans-fatty acids.

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When this occurs the beneficial effect can be nullified. This points to the importance of declarations on labels of the trans-fatty acid content. The only reservation to this is the conjugated fatty acids of dairy products, brought about by the rumen microbial activity, in which the molecule contains both cis and trans modification in adjacent pairs of C atoms in the carbon chain. The evidence indicates that conjugated fatty acids are generally recognized as safe. Health effects of Long chain N-3 fatty acids The three types of dietary essential omega-3 fatty acids involved in human physiology are a-linolenic acid (ALA) (found in plant oils)28,29,30, eicosapentaenoic acid (EPA), and docosahexaenoic acid (DHA) (both commonly found in marine oils). A meta-analysis31 showed a positive relationship between dietary cholesterol intake and serum cholesterol concentration; but surveys of any specific relationship between serum cholesterol concentration and the incidence of cardio-vascular disease (CVD) is weak. The reason for this is that the incidence of CVD is negatively associated with dietary fibre and vegetable protein intake which are also inversely associated with cholesterol intake. The risk of CVD is correlated with saturated fatty acid intake and the proportion of energy from fat, which in turn is positively associated with cholesterol intake. Nevertheless, saturated fatty acids are relatively stable in air, whereas foods containing unsaturated fatty acids are vulnerable to oxidation and rancidity when exposed to air if the foods are inadequately protected by natural or synthetic permissible antioxidants. The results of meta-analyses of surveys and prospective cohort studies indicate that the consumption of fish or fish oil, in which there are high concentrations of tocopherols and other natural antioxidants protecting the n-3 fatty acids, eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), is associated with decreased cardiovascular death, whereas consumption of the vegetable oil-derived n-3 a-linolenic acid is beneficial, but not as effective31,32,33. Randomized control trials (RCTs) in the context of secondary prevention indicate that the consumption of EPA plus DHA is protective at doses <1 g/d. The therapeutic effect appears to be due to suppression of fatal arrhythmias rather than stabilization of atherosclerotic plaques. At doses >3 g/d, EPA plus DHA can

improve cardiovascular disease risk factors, including decreasing plasma triacylglycerols (triglycerides), blood pressure (systolic and diastolic), platelet aggregation, and inflammation, while improving vascular reactivity33. Effects of Omega-3 Fatty Acids on Cardiovascular Disease Mainly on the basis of the results of RCTs, the American Heart Association recommends that everyone eat oily fish twice per week and that those with coronary heart disease eat 1 g/d of EPA plus DHA from oily fish or supplements34. Owing to the global scarcity of fish oil sources farmed fish at present contain less EPA or DHA, than do wild fish. This situation, we trust, will be rectified in due course by the development of a genetically modified Camelina sativa, as a land-based source of EPA and DHA by Haslam et al. (pages15-23). Inflammation Some research suggests that the antiinflammatory activity of long-chain omega-3 fatty acids may translate into clinical effects. A 2013 systematic review found tentative evidence of benefit35. Consumption of omega-3 fatty acids from marine sources lowers markers of inflammation in the blood, such as Creactive protein, interleukin 6, and TNF alpha. For rheumatoid arthritis (RA), one systematic review found consistent, but modest, evidence for the effect of marine n-3 PUFAs on symptoms such as â&#x20AC;&#x153;joint swelling and pain, duration of morning stiffness, global assessments of pain and disease activityâ&#x20AC;?35,36. However, the American College of Rheumatology has stated that there may be modest benefit from the use of fish oils, but that it may take months for effects to be seen, and cautions for possible gastrointestinal side effects and the possibility of supplements containing mercury or vitamin A at toxic levels37.

Sources of long-chain N-3 fatty acids The worldâ&#x20AC;&#x2122;s oceans are warming up. As the mean temperature of oceans rise it decreases their oxygen tension with a likely impact on wild fish stocks. This fact together with over-fishing to meet the demands of an everincreasing world human population, is leading to a depletion of these stocks, indicating the essentiality of fish farming. Fish, squid and krill are a good natural source of N-3 ( -3) fatty acids. However, these species are unable to

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scientific manufacture long chain N-3 fatty acids (EPA and DHA) to meet their needs. They depend on marine algae and phytoplankton as the primary sources of these fatty acids. These single cell organisms are the only significant source of EPA and DHA, required by both fish and humans, (although several bacterial genera have been identified as sources, e.g. Cellulophaga, Pibocella and Polaribacter in the Antarctic are able to produce EPA & DHA)38. The future of oceanic phytoplankton is unclear, owing to climate change. There are plant sources of shorter chain N-3 fatty acids e.g. alpha linolenic acid (ALA), including walnut, edible seeds, clary sage seed oil, algal oil, flaxseed oil, Sacha Inchi oil, Echium oil, and hemp oil. Fish and eventually Man depend on phytoplankton and the algae for the synthesis of long chain N-3 fatty acids in quantities to meet their nutritional requirements. The ability to transfer phytoplankton genes for the desaturase and elongase enzymes for the synthesis of EPA and DHA from shorter chain a-linolenic acid to false flax, described in this issue by Haslam and colleagues at Rothamsted, offers to potentially meet these needs without further destruction of the marine biosphere.

Omega-3 and omega-9 conclusions Overall, there is strong evidence that fish oils have a beneficial effect on blood triglycerides (neutral fat) that is dosedependent and similar in various populations33,39,40. There is also evidence of a very small beneficial effect of high doses (3-4g/d) fish oils on blood pressure41, especially that of DHA42 and possible beneficial effects on: coronary artery restenosis (stenosis-narrowing of the artery, restricting blood flow) after angioplasty43,44 and on exercise capacity in patients with coronary atherosclerosis, and possibly heart rate variability, particularly in patients with recent myocardial infarctions44, 45. No consistent beneficial effect is apparent for other analysed CVD risk factors or intermediate markers. However, there is also no consistent evidence of a detrimental effect of omega-3 fatty acids on glucose tolerance. The correlation between intake of omega-3 fatty acids and tissue levels is fairly uniform in different tissues46. Palm oil (from Elaeis guineensis L.) In this Issue we publish a paper on palm

CLA (Conjugated linoleic acid)

Table 1 Chemical composition of vegetable oils and butter (Moles %)47

Footnotes * Palm kernel oil is obtained from the kernel of the oil palm fruit. Vaccenic acidv, also known as (E)-Octadec-11-enoic acid is a C18.1 naturally occurring trans-fatty acid found in the fat of ruminants and in dairy products such as milk, butter, and yogurt. It is also the predominant fatty acid comprising trans fat in human milk48. The name was derived from the Latin vacca (cow). oil which contains approximately 44% palmitic acid and 37% oleic acid. As palmitic acid is fully saturated, and in an oil, a liquid at room temperature, it is more stable than many other oils, and so less subject to rancidity; but its saturated nature could have poorer health benefits than oils containing polyunsaturated fatty acids. Furthermore, its production has led to the destruction of vast areas of tropical forest. Nevertheless, it contains approximately 38% oleic acid, a monounsaturated fatty acid (Table 1), a fatty acid that has some putative health benefits. Olive oil (from Olea europaea L.) The Mediterranean Diet is one heavily influenced by monounsaturated fats. People in countries bordering the Mediterranean consume more total fat than those who live in Northern European countries, but most of the fat is in the form of monounsaturated fatty acids from olive oil and omega-3 fatty acids from fish, vegetables, and certain meats, while consumption of saturated fat is minimal in comparison. The diet in Crete is fairly high in total fat (40% of total energy, almost exclusively provided by olive oil) yet it affords a

remarkable protection from coronary heart disease49 (and probably colon cancer) ,owing, possibly to a very high oleic acid content50 (Tables 1 and 2). Much of the benefit may stem from the use of this oil in its uncooked form by Mediterranean countries. Although olive oil contains oleic acid at levels of 60-80% a major health benefit is thought to be the non-fat lipids (e.g. 0.2% phytosterol and tocosterols, hydroxytyrosol, oleuropein aglycone, and ligstroside along with traces of squalene (up to 0.7%) present only in the extra virgin oil). Olive oil is a source of at least 30 phenolic compounds, among which is elenolic acid, a marker for maturation of olives. The composition of a sample varies by cultivar, region, altitude, time of harvest, and extraction process (Table 2).

Table 2 Range in fatty acid composition of olive oil

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scientific Although epidemiological studies indicate that a higher proportion of oleic acid in the diet may be linked with a reduction in the risk of coronary heart disease a comprehensive scientific review by the European Food Safety Authority (EFSA)51 in 2011, concluded cause-and-effect relationships have not been adequately established for consumption of olive oil and for maintaining 1) normal blood LDL-cholesterol concentrations, 2) normal (fasting) blood concentrations of triglycerides, 3) normal blood HDL-cholesterol concentrations, and 4) normal blood glucose concentrations. But a large scale KANWU study52 found that increasing monounsaturated fat and decreasing saturated fat intake could improve insulin sensitivity, but only when the overall fat intake of the diet was low. Studies have shown that substituting dietary monounsaturated fat for saturated fat is associated with increased daily physical activity and resting energy expenditure53. More physical activity was associated with a higher-oleic acid diet than one of a palmitic acid diet. In children, consumption of monounsaturated oils is associated with healthier serum lipid profiles54. Limited and not conclusive scientific evidence suggests that eating about 2 tbsp. (23g) of olive oil daily may reduce the risk of coronary heart disease owing to the monounsaturated fat in olive oil. To achieve this possible benefit, olive oil is to replace a similar amount of saturated fat and not increase the total daily energy intake. In the United States, producers of olive oil may place a restricted health claim on product labels55. This decision was announced November 1, 2004, by the Food and Drug Administration after application was made to the FDA by producers. Similar labels are permitted for foods rich in medium chain omega-3 fatty acids such as walnuts and hemp seed. (A Summary of Qualified Health Claims Subject to Enforcement Discretion). But as mentioned above the low incidence of heart disease associated with a Mediterranean diet may owe, at least in part, to the non-fat, lipid constituents present only in extra virgin olive oil and the use of oil in the uncooked form, rather than as margarine.

Overall Conclusions 1. Vegetable oils are extracted mainly from seeds of: maize, soyabean, sunflower, linseed, rape, olive, and palm. There is concern over the effect of oil palm plantations on the destruction of wild life, reduction in biodiversity and damage to soil composition and structure, as well as

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the release of greenhouse gases during the initial clearance of the planting area. 2. The yield of oil/ha from the genetically improved oil-palm is very considerably greater than that, for example, of olives. 3. Vegetable oils provide over twice as much net energy/kg compared with starch and so their consumption can contribute to obesity with all its adverse effects on health. 4. Vegetable oils are a source of two dietary essential nutrients in the form of the polyunsaturated fatty acids (PUFA), C18:2, 6, linoleic acid and C18:3, 3, a-linolenic acid. Olive oil is also a rich source of C18:1, 9, oleic acid, a MUFA, which may contribute to its health benefits. 5. At present there has been no vegetable source of long chain omega3 dietary essential fatty acids C20:5, 3, eicosapentaenoic acid (EPA), and C22:6, 3, docosahexaenoic acid (DHA). Both these omega-3 fatty acids are essential in the diet of vertebrates, including fish and humans; but the only major source of them is the simple oceanic mono-cellular organisms, phytoplanktons and algae. Haslam et al. at Rothamsted describe in this Issue, their harvesting from these organisms the group of genes needed for the elongase and desaturase enzymes necessary for the production of EPA and DHA from a-linolenic acid, a C18:3, omega-3 acid.They have successfully incorporated these genes in the gene pool of Camelina sativa, false flax, a crop which can be grown in temperate climates. This will be an essential source for fish farming where their current source from wild fish oils, is becoming scarce. 6. There is now reasonable evidence that long chain omega-3 dietary essential fatty acids (C20:5, 3 and C22:6, 3), influence risk factors of cardio-vascular disease (CVD). The best evidence is that they are more potent than are the dietary essential, a-linolenic acid, an omega-3 acid (C18:3 3), linoleic acid an omega-6 acid (C18:2, 6), or than oleic acid, an omega-9 acid (C18:9, 1). All these unsaturated fatty acids are protective, as measured by risk factors to CVD, response; whereas saturated fatty acids, e.g. palmitic acid (C16:0), are considered to promote CVD, in comparison to a low fat diet56. Nevertheless, it should be remembered that palm oil is rich in both palmitic acid and oleic acid (Table 1). Olive oil contains a larger proportion of oleic acid and less palmitic acid that does palm oil, and is considered to be

protective, but the yield per ha of olive oil is far less than that of palm oil which has its environmental consequences! (see Murphy pages 2434). Unsaturated fats are prone to oxidation and rancidity, whereas saturated fats are relatively stable and the hydrogenation of unsaturated vegetable oils during the production of margarine leads to cis-trans isomerisation of unsaturated fats. The trans-isomers have been shown to raise plasma LDL cholesterol levels and to pose a risk for CVD. Hence, legislation has been introduced in the USA, where trans-fat levels must be declared on the labels of appropriate products in the USA. The relationship of fats to risk factors of CVD is well established and accepted. However the correlation of these risk factors with the occurrence of CVD is less well secure57 owing to the confounding of factors in mixed diets on the response of individuals. Some clarification of the situation is possible in the analysis of population studies.

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Disease: Implications for Nutrigenetics. J. Nutrigenet Nutrigenomics, 2 (3), 140–148. Published online 2009 Sep 23. doi: 10.1159/ 000235562 PMCID: PMC2820567 26 Schwingshackl, L. and Hoffmann, G. (2012) Monounsaturated Fatty Acids and Risk of Cardiovascular Disease: Synopsis of the Evidence Available from Systematic Reviews and MetaAnalyses. Nutrients 4 (12), 1989–2007. Published online 2012 Dec 11. doi: 10.3390/nu4121989 PMCID: PMC3546618 27 Frape, D.L., Williams, N.R., Carpenter K, Freeman, M.A., Palmer C.R. and Fletcher, R.J. (2000) Insulin response and changes in composition of nonesterified fatty acids in blood plasma of middle-aged men following isoenergetic fatty and carbohydrate breakfasts. British Journal of Nutrition 84, 737-745. 28 Pan A., Chen M, Chowdhury R, Wu J.H, Sun Q, Campos H, Mozaffarian D, Hu FB (2012) aLinolenic acid and risk of cardiovascular disease: a systematic review and meta-analysis. Am J Clin Nutr., 96 (6):1262-73. doi: 10.3945/ajcn. 112.044040. Epub 2012 Oct 17. 29 Rodriguez-Leyva, D. Bassett, C.M.C., McCullough, R. and Pierce, G.N. (2010) The cardiovascular effects of flaxseed and its omega-3 fatty acid, alphalinolenic acid. Can J Cardiol. 26 (9): 489–496. PMCID: PMC2989356. 30 Pan A, Chen M, Chowdhury R; et al. (2012). aLinolenic acid and risk of cardiovascular disease: a systematic review and meta-analysis. Am. J. Clin. Nutr. (Systematic review) 96 (6): 1262–73. doi:10.3945/ajcn.112.044040. PMC 3497923. PMID 31 Marchioli, R. and Levantesi, G.(2013) n–3 PUFAs in cardiovascular disease. Proceedings from the Round Table on “Current evidence and future perspectives on n–3 PUFA” London, UK, 2012. International Journal of Cardiology, 170, (2) Supplement 1, S33–S38 Ed. Francesco Pelliccia S0167527313X00361-cov150h.gif 32. Mozaffarian, D.and,Wu, J. H.Y.(2011) Omega3 Fatty Acids and Cardiovascular Disease : Effects on Risk Factors, Molecular Pathways, and Clinical Events. Journal of the American College of Cardiology, 58, (20), 2047–2067. 33 Anon. Agency for Healthcare Research and Quality ( AHRQ) U.S. Departmentof Health & Human Services (2004) Effects of Omega-3 Fatty Acids on Cardiovascular Disease Evidence Report/ echnology Assessment: Number 94. www.ahrq.gov., www.hhs.gov AHRQ, Archived EPC Evidence Reports, Publication No. 04-E009-2 March 2004 34 Anon. The American Heart Association (2015) Eating fish for heart health, Tweet 29, updated 15th May,2015, 7272 Greenville Ave. Dallas, TX 75231, Customer Service, 1-800-AHA-USA-1, 1800-242-8721 35. Di Giuseppe, D., Wallin, A. Bottai, M., Askling, J. and Wolk, A. (2013) Long-term intake of dietary long-chain n-3 polyunsaturated fatty acids and risk of rheumatoid arthritis: a prospective cohort study of women Ann Rheum Dis doi:10.1136/ annrheumdis-2013-203338 Clinical and epidemiological research 36 Calder PC (2008). Symposium on ‘Nutrition and autoimmune disease’ PUFA, inflammatory processes and rheumatoid arthritis. Proc Nutr Soc. 67 (4), 409-18. doi: 10.1017/S0029665108 008690. Session 3: Joint Nutrition Society and Irish Nutrition and Dietetic Institute 37 Geusens P., Wouters, C. Nijs, J.,Jiang Y. and Dequeker J.(2005) Long-term effect of omega-3 fatty acid supplementation in active rheumatoid arthritis Arthritis & Rheumatism 37, (6), 824–829, Article first published online: 9 DEC 2005 DOI: 10.1002/art.1780370608 Copyright © 1994 American College of Rheumatology. 38 Bianchi, A. C., Olazábal, L, Torre, A. and Loperena, L (2014) Antarctic microorganisms as

source of the omega-3 polyunsaturated fatty acid. World Journal of Microbiology and Biotechnology. 30 (6) 1869-1878. First online: 29 January 2014. 39 Svensson M., Christensen J.H., Sølling J., Schmidt E.B.(2004) The effect of n-3 fatty acids on plasma lipids and lipoproteins and blood pressure in patients with CRF. Am J Kidney Dis. 44 (1) 7783. 40 Boberg M., Pollare, T., Siegbahn, A., Vessby, B. (1992) Supplementation with n-3 fatty acids reduces triglycerides but increases PAI-1 in noninsulindependent diabetes mellitus. Eur J Clin Invest. 22 (10), 645-50. 41. Massaro, M., Scoditti, E., Carluccio M.A., Campana M.C. and De Caterina, R. (2010) Omega-3 fatty acids, inflammation and angiogenesis: basic mechanisms behind the cardioprotective effects of fish and fish oils. Cell Mol. Biol. (Noisy-le-grand). 56, (1), 59-82. 42 Mori T.A., Bao D.Q., Burke V, Puddey I.B. snd Beilin L.J. (1999) Docosahexaenoic acid but not eicosapentaenoic acid lowers ambulatory blood pressure and heart rate in humans. Hypertension. 34 (2), 253-60. 43 Dehmer, G.J., ,Popma,J.J.,van den Berg, E.K.., Eichhorn, E.J.,Prewitt, J.B.,. Campbell, W.B. et al.., (1988) Reduction in the Rate of Early Restenosis after Coronary Angioplasty by a Diet Supplemented with n–3 Fatty Acids. N Engl J Med, 319, 733-740. DOI: 10.1056/NEJM1988092 23191201 44 Balk, E.M, , Lichtenstein, A.H., Chung, M, Kupelnick, B., Chew P and Lau, J. (2006) Effects of omega-3 fatty acids on coronary restenosis, intima– media thickness, and exercise tolerance: A systematic review. Atherosclerosis 184 ,(2), 237– 246. 45 Anon. (2004) U.S. Department of Health & Human Services, www.hhs.gov; Agency for Healthcare Research and Quality AHRQ, Archived EPC Evidence Reports Effects of Omega-3 Fatty Acids on Cardiovascular Risk Factors and Intermediate Markers of Cardiovascular Disease Evidence Report/Technology Assessment: Number 93 46 Garneau,V., Rudkowska, I,, Paradis, A.M., Godin, G., Julien, P., Pérusse, L., and Vohl, M.C. (2012) Omega-3 fatty acids status in human subjects estimated using a food frequency questionnaire and plasma phospholipids level. Nutr J.,11, (46), doi: 10.1186/1475-289. 47 Anon. (1976) online edition: Fat Content and Composition of Animal Products, Nutrient database, Release 24. United States Department of Agriculture. Publishing Office, National Academy of Science, Washington, D.C., ISBN 0-309-02440-4; p. 203. 48 Friesen, R., and Innis, S.M. (2006) Trans Fatty acids in Human milk in Canada declined with the introduction of trans fat food labeling, J. Nut., 136, 2558-2561). 49. Guasch-Ferré, M., Hu, F.B., Martínez-González, M.A., Fitó, M., Bulló,M, Estruch,R, Ros, E., Corella D. et al, (2014) Olive oil intake and risk of cardiovascular disease and mortality in the PREDIMED Study. BMC Medicine, 12, (78) doi:10.1186/1741-7015-12-78 50 León, L., Uceda, M., Jiménez, A., Martín, L.M. and Rallo, L. (2004) Variability of fatty acid composition in olive (Olea europaea L.) progenies. Spanish Journal of Agricultural Research 2 (3), 353-359 51 Anon. Scientific Committee/Scientific Panel of the European Food Safety Authority. (2011) Scientific Opinion on the substantiation of health claims related to olive oil and maintenance of normal blood LDL-cholesterol concentrations EFSA Journal (European Commission) 9 (4), 2044 [19 pp]. doi:10.2903/j.efsa.2011.2044. Retrieved April 5, 2013. 52 Vessby B, Uusitupa M, Hermansen K, Riccardi G, Rivellese A .A, Tapsell L .C, Nälsén C, Berglund

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scientific L, Louheranta A, Rasmussen B .M, Calvert G .D, Maffetone A, Pedersen E, Gustafsson I .B, Storlien L .H. (2001) Substituting dietary saturated for monounsaturated fat impairs insulin sensitivity in healthy men and women: The KANWU Study. Diabetologia,.44 (3), 312-9. 53 Kien, C.L., Bunn, J.Y., Tompkins, C.L., Dumas, J.A., Crain, K.I., Ebenstein, D.B., Koves, T.R. and Muoio, D.M. (2013). Substituting dietary monounsaturated fat for saturated fat is associated with increased daily physical activity and resting energy expenditure and with changes in mood. The American Journal of Clinical Nutrition 97 (4), 689â&#x20AC;&#x201C;697. doi:10.3945/ajcn.112.051730.

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PMID 23446891). 54 Sanchez-Bayle M., Gonzalez-Requejo A., Pelaez M.J., Morales M.T., Asensio-Anton J. and AntonPacheco E. (2008). A cross-sectional study of dietary habits and lipid profiles. The RivasVaciamadrid study. Eur. J. Pediatr. 167 (2), 149â&#x20AC;&#x201C;54. doi:10.1007/s00431-007-0439-6. PMID 17333272.). 55 U.S. Food and Drug Administration (2004) Monounsaturated Fatty Acids From Olive Oil and Coronary Heart Disease. Summary of Qualified Health Claims Subject to Enforcement Discretion. Docket No. 2003Q-0559 11/01/2004 enforcement discretion letter.

56 Frape, D.L., Williams, N.R., Rajput-Williams, J. Maitland, B.W., Fletcher, R.J. and Palmer, C.R. (1998). Circadian variation in blood thrombogenic characteristics in middle-aged healthy men given isoenergetic carbohydrate and fatty breakfasts. Fibrinolysis & Proteolysis, 12, 311-319. 57 Rizos, E.C., Ntzani, E.E., Bika, E., Kostapanos, M.S. and Elisaf, M.S. (2012) Association Between Omega-3 Fatty Acid Supplementation and Risk of Major Cardiovascular Disease Events: A Systematic Review and Meta-analysis. JAMA, 308 (10),1024-1033. doi:10.1001/2012.jama.11374.

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The supply of fish oil to aquaculture: a role for transgenic oilseed crops? Richard P Haslam1, Sarah Usher1, Olga Sayanova1, Johnathan A Napier1, Monica B Betancor2, Douglas R Tocher2 1 Biological Chemistry & Crop Protection, Rothamsted Research, Harpenden, Hertfordshire, AL5 2JQ, UK. 2 Institute of Aquaculture, School of Natural Sciences, University of Stirling, Stirling FK9 4LA, Scotland, UK. Authors for correspondence: Richard Haslam, richard.haslam@rothamsted.ac.uk; Douglas Tocher, d.r.tocher@stir.ac.uk Summary The importance of an alternative and sustainable supply of omega-3 long chain polyunsaturated fatty acids (LC omega-3) has long been established. As these biologically active fatty acids have a role in nutrition and health, there is an ever increasing demand for oils containing LC omega-3 e.g. eicosapentaenoic (EPA) and docosahexaenoic acid (DHA). These fatty acids are produced by micoroganisms and enter our diet through the consumption of fish. However, in order that the nutritional requirements of fish in aquaculture are met and sufficient levels are deposited to meet the requirements of human consumers, EPA and DHA must be supplied in excess. Given the importance of the aquaculture industry in delivering healthy foodstuff, the question of how to resource the supply of LC omega-3 then arises; traditional sources of EPA and DHA (fish oil) are challenged, whilst vegetable oils do not contain EPA or DHA. Therefore research efforts have focused on the successful reconstitution of LC omega-3 biosynthesis in oilseed crops. The production of EPA and DHA in the seed oil of agricultural crops has the capacity to deliver large volumes of these fatty acids. The expression of optimised combinations of the genes required to produce these fatty acids in the seed of the crop Camelina sativa has been achieved and the utility of this approach demonstrated. This represents a significant breakthrough – the provision of an effective alternative to the use of omega-3 fish oil by the global aquaculture industry. Key words Aquaculture; fish oil; nutrition; metabolism; sustainability; GM plants; Omega-3; plant biotechnology Abbreviations CVD, cardiovascular disease; DHA, docosahexaenoic acid (22:6n-3); EFA, essential fatty acid; EPA, eicosapentaenoic acid (20:5n-3); FM, fishmeal; FO, fish oil; GM, genetically modified; LC-PUFA, long-chain polyunsaturated fatty acids (≥C20 ≥ 3 double bonds); LC omega-3, LC-PUFA predominantly EPA and DHA; MT, metric million tonnes; TAG, triacylglycerol; VO, vegetable oil.

Introduction

n 2010, fish accounted for around 17% of the global population’s intake of animal protein and almost 7% of all protein consumed (1). As well as being an important dietary sources of protein, minerals and vitamins (2), fish and seafood are also the major sources of long chain (LC) omega-3 polyunsaturated fatty acids, particularly eicosapentaenoic (EPA; ) and docosahexaenoic (DHA; ) acids (3), that have wellknown beneficial effects in human health, including cardiovascular and inflammatory diseases, and important roles in neural development (4,5). However, global marine fisheries are stagnating and over 60% of fish stocks require rebuilding (6) so that an increasing proportion of fish are

farmed, reaching almost 50% in 2012 (1). Paradoxically, feeds for many farmed fish species are dependent on fishmeal and fish oil, themselves derived from marine fisheries, for the supply of LC omega-3 (7). Reliance on finite marine resources was an unsustainable practice (8) and the continued growth of aquaculture has been dependent upon the development of more sustainable feeds with alternative ingredients, generally derived from terrestrial agriculture, that lack LC omega-3 (9). This has important consequences for the supply of these nutrients to human consumers and so there has been a global drive to find alternative supplies of LC omega-3 fatty acids for aquaculture (10). The most promising and viable

option for entirely new sources of LC omega-3 are transgenic oilseed crops.

2. Long chain omega-3 and human health It has long been appreciated that dietary LC omega-3 can have important, generally beneficial effects on human health (11). The strongest evidence has been found in relation to heart and cardiovascular disease (CVD) (12); today a large number of national health agencies and government bodies recognize the importance of increasing dietary intake of EPA and DHA to promote cardiac health and decrease the risk of CVD (12,13). Recently, the current advice and guidelines worldwide were compre

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Table 1 International recommendations for dietary long-chain n-3 LC-PUFA consumption in humans. ALA, linolenic acid; DHA, docosahexaenoic acid; EPA, eicosapentaenoic acid; FAO, Food and Agriculture Organization; ISSFAL, International Society for the Study of Fatty Acids and Lipids; NATO, North Atlantic Treaty Organization; WHO, World Health

hensively reviewed (14) and recommendations of over 50 organisations were compiled by the Global Organisation for EPA and DHA (15). Most recommendations suggest between 250 and 500 mg/d of EPA and DHA for reducing CVD risk or 1 g/d for secondary prevention in existing CVD patients, with a dietary strategy for achieving 500 mg/d being to consume two fish meals (200 – 250g) per week with at least one of oily fish (14,16,17) (Table 1). In addition to cardiac health and CVD, dietary LC omega-3 can be beneficial in several other pathologies with the most robust evidence for inflammatory diseases obtained in rheumatoid arthritis, in which the dose required to gain benefit is set higher than for CVD (around 3g per day (18)). There is also increasing evidence for beneficial effects of dietary LC omega-3 in Inflammatory Bowel Diseases (IBD) such as Crohn’s disease and ulcerative colitis (19). The effects of dietary LC omega-3 on cancers has been more controversial. Epidemiological studies indicated that, in general, dietary LC-omega-3 may decrease risk of colo-rectal, breast and prostate cancers (20) and some studies suggest beneficial effects in chemotherapy (21). However, one research group suggested that LC-omega-3 may be associated with increased risk of prostate cancer (22,23); although latterly a second systematic review and meta-analyses of all studies concluded

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that the results did not support an association between LC omega-3 and prostate cancer (24). With regard to development, there is robust evidence that decreased DHA status can lead to cognitive and visual impairment and that DHA supplements have positive beneficial outcomes in pre-term infants (25). There have also been several reports of potential beneficial effects of dietary DHA supplementation in a number of psychological/behavioural/ psychiatric disorders including attention deficit hyperactivity disorder and depression, although there are insufficient studies and data to draw firm conclusions (26). However, it is becoming generally recognised that LC omega-3 are potential key nutrients to prevent various pathological conditions associated with the normal aging process (27), which has prompted research into the effects of LC omega-3 on dementia, including Alzheimer’s disease and other age-related cognitive impairments (28). In general, DHA supplementation trials in patients with some pre-diagnosed cognitive impairment indicated that this appeared to slow progression of Alzheimer’s (29).

3. Aquaculture: requirement for LC omega-3 Vertebrates, including fish, cannot synthesise polyunsaturated fatty acids (PUFA) because they lack the enzymes required for their production from monounsaturated fatty acids and so they are essential in the diet.

Terrestrial plants can be rich in medium chain PUFA such as linoleic acid ( ) and linolenic acid (LNA, ), but the biologically active fatty acids in fish are the long-chain PUFA, primarily EPA and DHA. Some freshwater and salmonids species of fish can produce EPA and DHA from LNA, but most marine fish cannot. In consequence, which PUFA can satisfy the essential fatty acid (EFA) requirements in fish vary with species (30,31). The actual EFA requirement in fish can be described at three levels. The amount of EFA a fish requires to prevent nutritional pathology is low, often around 1% of the diet (30,31). However, a higher level of EFA may be required to support optimum growth and health, which is similar to the situation in humans where few people suffer from EFA deficiency but, rather, LC omega-3 is required for optimal development and health. The final EFA requirement level in fish is that to maintain nutritional quality based on LC omega-3 content of the flesh (9). As such, this is not a requirement of the fish, but rather that of human consumers (32). To satisfy this level, EPA and DHA need to be supplied to the fish well in excess of the requirements for optimal health and growth so that they are deposited and stored in the fish. For example, to produce farmed salmon with the level of EPA and DHA required to supply the weekly human requirement of 3.5g in one 130g portion, it would be necessary for EPA plus DHA to be at 6-7% of diet (33).

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scientific This level of supplementation would make fish-farming commercially uneconomical.

4. Fish Oil In 2013 around 75% of total global fish oil supply was used in aquaculture, with 83% of that consumed by salmonids (60%) and marine fish (23%), and a further 21% used for direct human consumption (34) (Figs.1A &B). Despite continued growth of aquaculture (1), the use of fish oil for feeds has been relatively stable over the last decade with, on average, around 0.8 million metric tonnes (Mt) being used (34) (Fig.1C). The primary constraint with fish oil is that it is a finite resource with production limited through strict regulation of fishing and catch quotas (35,36). Although production of fish oil has declined in recent years, largely due to regulation and quotas in South America (37), this has been partially offset by increased use of seafood and aquaculture byproducts including by-catch and trimmings to produce fish meal and, to a lesser extent, fish oil (36). However, fish oil production averages around 1 million Mt annually and there is little to no prospect of that increasing. Production of fish oil is also subject to environmental influences and acute phenomena such as El Ni単o have wellknown consequences, considerably reducing supply (38). Sustainability issues are also key drivers limiting fish oil supplies, and these will have an increasing impact with the many

Table 2. World oil and fat production in 2012 (a). a http://lipidlibrary.aocs.org/market/ ofo6-07.htm (Updated 03/2013;

Figure 1. Global Consumption and supply of fish oil. In 2013 around 75% of total global fish oil supply was used in aquaculture, 83% of that consumed by salmonids (60%) and marine fish (23%), and 21% went human consumption (a & b). The use of fish oil for feeds has been relatively stable over the last decade on average around 0.8 million metric tonnes (34) (c).

initiatives currently being developed with respect to both national and international standards and certification of marine ingredients, including fish oil (33). Although increasing adoption and implementation of these standards will further improve sustainability, they will 16:0

likely have impacts on the availability of fish oil and its use in aquaculture. A further factor constraining the use of fish oil is the presence of contaminants/undesirables such as persistent organic pollutants (POPS) including dioxins and PCBs (9,39). With some fish oils, such as those from 18: 2n-6

Table 3. Fatty acid (FA) composition (Mol%) of major vegetable oils and animal fats. *Sat.,saturated FA; Mono., monounsaturated FA

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RO b

aquaculture and algal sources. The calculations in Table 5 contain assumptions and estimates and so the precise extent of the difference can be the argued, however, that there is a gap between supply and demand is not in question irrespective of how it is calculated (42). There is a fundamental, global lack of LC omega-3 to supply human needs, whether by direct consumption or via aquaculture.

5. Alternative sources of omega-3 LC-PUFA There is an urgent need for alternative sources of the LC omega-3, EPA and DHA (41). As the primary producers of almost all LC omega-3 are marine microalgae and bacteria, the only alternatives to traditional fish oil are other oils sourced from the marine environment including lower trophic levels (zooplankton), mesopelagic fish, by-catch/ by-products and microalgae themselves.

Table 4 Effect of complete or partial replacement of dietary fish oils by vegetable oils on fatty acid compositions (percentage of weight of total lipid) of flesh of Atlantic salmon. FO, fish oil; LO, Linseed oil; PO, palm oil; RO, rapeseed (Canola) oil; SO, sunflower oil; VO, vegetable oil blend.Details of fish initial weight, extent of dietry replacement and length of feeding trial are provided: a Initial wt. 55 g / 100 % replacement / 30 weeks, b Initial wt. 80 g / 100 % replacement / 17 weeks, c Initial wt. 22 g / 100 % replacement / 9 weeks, d Initial wt. 127 g / 100 % replacement / 40 weeks), e Initial wt. 0.16g / 100 % replacement, RO/PO/LO [3.7:2:1] / 22 months.

the Baltic, levels can be higher than permitted for use in animal feeds and these require decontamination before they can be used. However, this is an issue that has been diminishing to some extent with the increasing replacement of dietary fish oil and as a result levels of these undesirable marine environmental contaminants in feeds are decreasing (40). To put demand for fish oil (viz. LC omega-3) for aquaculture into perspective, to supply the salmon industry alone would require more than 1 million Mt annually (i.e. greater than the average global supply). Thus the only way aquaculture has continued to grow has been by increasing substitution with alternative oils (10). Global oil and fat production was more than 185 million Mt in 2012, with total production of vegetable oils at over 160 million Mt, and animal fats including tallow, lard and butter totalling another 25 million Mt. Thus, alternative oils are plentiful although they all lack LC omega-3 (Table 2). Terrestrial plants do not

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produce EPA and DHA and so they are not components of any vegetable oil, whilst animal fats are dominated by saturated and monounsaturated fatty acids with only low levels of PUFA (Table 3). The consequence of this has been the increasing substitution of fish oil with alternative oils, effectively spreading the available fish oil thinner in the feeds, which has inevitably led to a reduction in LC omega-3 levels in both feeds and farmed fish (10) (Table 4). However, the issues surrounding the limited supply of LC omega-3 transcend aquaculture. Based on the most commonly recommended dose for cardiac health (500 mg/day (15)), the demand for LC omega-3 is over 1.25 million Mt whereas global supply is optimistically estimated at just over 0.8 million Mt indicating a shortfall of over 0.4 million Mts (41) (Table 5). The majority of supply (almost 90%) is from capture fisheries, whether as food fish or via fish oil and meal, with small additional amounts estimated from seafood by-products, unfed

Lower trophic levels Zooplankton such as krill and calanoid copepods in the southern and northern hemispheres, respectively, are possible options but, although biomass at lower trophic levels is large, there are inherent dangers associated with fishing down the marine food web (43). Potentially, zooplankton can be good oil sources, but harvesting of krill and copepods poses significant technological challenges and cost (44). For most species, lack of schooling behaviour makes harvest by traditional trawling technology an expensive economic option (44). Antarctic krill, which do form schools, are the only species being targeted for commercial harvest, apart from a small scientific quota (~1000 Mt) of the calanoid copepod, Calanus finmachicus (45). Krill meals, that contain residual oil and therefore some LC omega-3, are currently used in some premium feeds focussed on health benefits and are generally used sparingly. These krill meals are therefore not being used as primary sources of LC omega-3 and, currently, krill oils are used almost exclusively for the human nutraceutical market. Although there may be evidence that harvesting krill, and potentially copepods, could be sustainable, there are still significant environmental and ecological concerns (44). For instance, Antarctic krill are near the base of a food chain that

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scientific Liver from species like cod and halibut have traditionally been used for fish oil production, but production is now relatively small (~ 40,000 Mt) and goes mostly for direct human consumption as vitamin supplements as much as sources of LC omega-3 (54). Oil is now being actively recovered from aquaculture species waste, particularly salmon farming, with around 20,000 Mt reportedly recovered in Norway (55) and 50,000 Mt in Chile in 2006 (56).

Table 5. Potential annual demand for n-3 LC-PUFA based on recommended intake for reduction of risk of cardio-vascular disease compared with global annual supply from major sources. Production figures are from 2012 (FAO, 20141). All lipid and n-3 LC-PUFA contents/yields are estimated averages over the wide range of species in each category. 1Salmonids include salmon and trout spp. Freshwater species includes eels, tilapia and other freshwater species that still utilise some fishmeal and fish oil (13% of total fish oil used in aquaculture) in feeds. NA, not available. Although there will be some endogenous production of n-3 LC-PUFA inversely related to fishmeal and oil contents of feeds, this cannot be accurately estimated, but will likely be minor based on volume of fish oil consumed by these sectors (75% of all fish oil used in aquaculture).

includes whales and penguins, suggesting there could be damage to marine biodiversity (46). Mesopelagic fish Mesopelagic fish that inhabit the intermediate pelagic water masses between the euphotic zone at 100m depth and the deep bathypelagic zone at 1000m are available in potentially large quantities (1-6 billion Mt), with lantern fish, myctophids, constituting about 60% of biomass (47). Different species can contain between 16 and 60% of dry weight (48) as oil and most are potentially good sources of LC omega-3 (44). On the positive side, they are resources that, so far, have not been the subject of commercial exploitation, and they do not compete with existing or potential human feed production. Negative points include biological (seasonal variation), ecological (mixed fishery difficult to manage), technical (capture methods and on-board processing), and nutritional issues. By-catch and seafood processing by-products In almost all fisheries there are non-

target catch and/or discarded target catch that, together, make up the by-catch. However, both the precise definition and resultant estimates of by-catch can be controversial (49). In 2005, the discard rate was estimated at around 7 million Mt/year or 8% of the global catch (50). By its nature, by-catch is a diffuse resource (51) and this imposes a major limitation to its usefulness as a source of fish oil, although processing of by-products, including oil production, at sea is an increasing trend (52). Another limitation is that by-catch includes a multitude of species, not necessarily â&#x20AC;&#x153;oilyâ&#x20AC;?, which limits the quantity and quality of the oils produced (51). Seafood industry by-products including viscera, heads, carcasses and trimmings, particularly those produced from pelagic fisheries and aquaculture are another potential source of marine oil although this is largely dictated by species. Thus, by-products from oily species including salmon, herring and mackerel can be a source of substantial oil whereas by-products from other pelagic (white fish) fisheries have generally low oil contents (53).

Marine microalgae Potentially, culture of the main primary producers, marine microalgae, could offer a long-term solution to the sustainable supply of LC omega-3 (57). Various photosynthetic microalgae are already commonly used in fish hatcheries to supply both EPA (e.g. diatoms) and DHA (e.g. flagellates) in the rearing of larval marine crustacean and fish species (58). Production usually employs medium- to highdensity batch, semi-continuous or continuous culture in relatively small volumes (59). Up-scaling of production to the volumes required for algal oil and/or algal biomass to supply the amount of LC omega-3 required to replace fish oil in commercial aquafeed production has significant biological and technological challenges (60). Economic production of LC omega-3 would require algae to demonstrate simultaneous high growth and high oil content with high proportions of EPA and DHA. These are almost exclusive traits as oil deposition is usually associated with conditions which occur only when growth is limited (e.g. nitrogen limitation) (61). Technical challenges include efficient capture of light energy in high-density culture with effective temperature control. These issues remain to be solved but there are several research strategies targeting their solution. These include exploiting culture conditions to direct metabolism towards lipid production, to improve biomass productivity or oil yield by mutagenesis and selective breeding, and to improve strains by genetic modifications to optimize light absorption and increase biosynthesis of EPA and DHA (60). Therefore, in the future, algal species with favourable biological characteristics may be found and/or developed, and photobioreactor technologies may improve considerably enabling economically sustainable production of microalgae rich in EPA and DHA for use in

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scientific aquafeed. In contrast, heterotrophic microalgae species including Crypthecodinium and thraustochytrids such as Schizochytrium are already being utilised for the commercial production of DHA using large-scale biofermentor technology (62). Even so, the high production costs are generally limiting the use of these products to direct human consumption mainly in the form of DHA supplementation of infant formulae (63). However, the DHA-rich products from heterotrophic microalgae may have niche markets in marine hatcheries, particularly for high-value species. Production volumes would have to be increased and costs reduced before these products could be viable for wider application in aquaculture.

6. Plants as a source of omega-3 LC-PUFA It has long been the hope of researchers in the field of plant lipid biotechnology to produce a terrestrial supply of vegetable oil with a composition (EPA/DHA) matching that of fish oil. However, metabolic engineering on this scale is not trivial. Synthesis of LC omega-3 commonly occurs in marine microalgae via a series of sequential aerobic desaturation and elongation reactions. These reactions typically follow two routes – the ‘D6 pathway’ (Fig 2a) beginning with the D6-desaturation of the C18 substrate, C2 elongation and D5-desaturation or the much rarer ‘D8 pathway’ where the C18 substrate undergoes a C2 elongation, followed by two rounds of desaturation. To then generate DHA in either pathway requires a further C2 elongation and desaturation. Through whichever aerobic route, a minimum of three genes are required to synthesise EPA and five for DHA production. A further anaerobic route to LC omega-3 has been identified in some bacteria and unicellular marine eukaryotes and functionally characterised; this pathway uses a processive polyketide synthase-like enzymatic system to convert malonyl-CoA to EPA and DHA with the production of no intermediates (64,65). The activities and genes for each of the biochemical routes to LC omega-3 FA production have been characterised and are available for use by the metabolic engineer to reconstitute EPA/DHA synthesis in a suitable heterologous host (64). However, success can only be

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Figure 2. The biosynthesis pathway of LC omega-3 in Camelina. (a) Schematic representation of the enzymatic steps involved in the synthesis of LC omega-3 fatty acids; total fatty acid composition of generic fish oil (b) and an individual seed of GM Camelina (72).

achieved by addressing some significant challenges: (1) the C18 dior tri-unsaturated substrate must be pre-existing; (2) reconstitution of the pathway in a specific tissue (e.g. seed) requires the co-ordinated and targeted expression of multiple genes and activities; (3) the production of novel LC omega-3 and their correct acyl-exchange between lipid pools depends on the capacity of native endogenous enzymes that are unfamiliar with the fatty acids; and (4) the processes underpinning the biochemical acyl-exchange or flux of fatty acids between lipid species within plant cells is only now starting to be appreciated. It is entirely possible for biosynthetic intermediates to be channelled into ‘metabolic cul-de-sacs’ rendering them unavailable for further desaturation, elongation or storage in seed oil (65). Historically, many of the individual genes necessary for LC omega-3 production were individually characterised in plants, indicating that in combination they would be successful. The first demonstration of EPA production in a transgenic plant was published by Qi et al. (66) expressing the algal alternative pathway in the leaves of Arabidopsis thaliana. The approach used a series of sequential transformations of individual genes and resulted in the vegetative accumulation of EPA, predominantly in phospholipids. To be of economic value in the context of aquaculture as described above, it is necessary to have an engineered oilseed crop where the target LC omega-3 would be produced and stored in the neutral lipids (triacylglycerol) of seeds at high levels. The possibility of LC omega-3 biosynthesis targeted to seeds was shown by Abbadi (67) in which the

conventional D6 pathway was expressed in transgenic linseed. Abbadi (67) identified the presence of low levels of EPA in seeds, but concomitant with high levels of C18 D6-intermediates. The un-wanted intermediates were the result of the poor acyl-exchange of intermediates between the acyl-CoA pool (elongation) and glycerolipid pool (desaturation). Following these proofof-concept studies efforts have continued to drive up the accumulation of LC omega-3 in seed oil and reduce the presence of intermediates e.g. D6 desaturation products like linolenic acid. Such iterative engineering followed two strategies, the first utilised by Petrie and co-workers (CSIRO) made use of Agrobacterium-mediated transient expression of multiple gene combinations in Nicotiana benthamiana (68). Although testing was undertaken in leaves, the co-expression of the Lec2 transcription factor or master regulator essentially ‘reprogrammed’ the leaf to replicate the lipid composition of a seed; a system that permitted the rapid selection of optimal gene combinations. The second approach, adopted by Heinz et al. (University of Hamburg) and Napier et al. (Rothamsted Research) was to directly assess gene combinations and their regulatory elements in the seeds of stably transformed plants (namely the oilseed model A. thaliana) (69,70). In combination with the development lipidomic approaches, it then enabled the evaluation of gene combination efficacy in the seed. Critical to the progress of these efforts was the use of omega-3 desaturases (reducing the accumulation of un-wanted omega-6 fatty acids) and the use of acyl-CoA dependent desaturases (breaking the

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scientific desaturase/elongase substrate dichotomy) (65).

7. Transition to crops As described, the majority of the systematic work undertaken to produce a seed oil composition akin to fish oil (i.e. ~20% EPA and DHA in total fatty acids) was undertaken in model plant species i.e. arabidopsis and tobacco. However, to produce the volumes of LC omega-3 required by aquaculture necessitates the production of EPA and DHA in agricultural oilseed crops. The opportunities of scale associated with such crops provide the only chance to generate a fish oil substitute in significant quantities. From the available oilseed crops, screening has identified two as appropriate hosts for the production of LC omega-3; the first canola, a cultivar of rapeseed (Brassica napus L.) and secondly Camelina (Camelina sativa L). At this time no public data are available to assess the expression of the LC omega-3 trait in canola. However, two laboratories (Rothamsted and CSIRO) have demonstrated the success of Camelina as a host for the accumulation of EPA and DHA in seed oil (71,72). Camelina is an oilseed crop of the Brassicaceae adapted to temperate growing regions, with a low input requirement, short crop cycle and disease resistance. In terms of performance, Camelina has an acceptable yield (levels over 3000 kg/ha have been achieved) with an oil content of ~40%. Of interest to metabolic engineers, Camelina is an excellent platform for the production of tailored oils; it has very low outcrossing levels, and fully developed tools for breeding and molecular trait improvement due to the high sequence identity with Arabidopsis. Furthermore, genetic transformation is possible using Agrobacterium-mediated floral dip. However, it is the unique fatty acid composition of Camelina (unusual for a Brassicaceae the polyunsaturated linolenic acid (18:3) and linoleic acid (18:2) – substrates for LC omega-3 synthesis – are the major fatty acids, whilst erucic acid (22:1) is low) that engenders this host to genetic engineering approaches (73). Although different approaches were taken by Rothamsted and CSIRO, both demonstrated the suitability of Camelina as a host for the production of LC omega-3 in seeds. Researchers at Rothamsted used knowledge acquired from earlier engineering in Arabidopsis, introducing two optimised constructs

into Camelina – one producing EPA alone and the other making both EPA and DHA. Analysis of the seed fatty acid composition from the stable transgenic lines revealed the average level of EPA alone was 24%, and for EPA and DHA, 11 and 8% respectively (72). Significantly in both constructs only very low levels of C18 intermediates were recorded. Overall, the average total level of LC omega-3 was 19% (EPA + DHA) and much higher (25%) in some single seeds (see Fig 2) (72). The reported work from CSIRO showed significant accumulations of DHA with all the introduced constructs (12% with construct combination GA7 and mod-F), however levels of EPA were low (~3% for mod-F) (71). The differences in the accumulations of LC omega-3 in Camelina can be attributed to a number of factors e.g. selection of seed-specific promoter, choice of Camelina variety, activity of each enzyme choice, constructs design/ orientation, and possibly site of integration. For example, it is likely that the use of a highly active D5elongases resulted in the specific difference in EPA accumulation (65). Moreover, field evaluation of the LC omega-3 trait (EPA + DHA) in Camelina was undertaken at Rothamsted, where the feasibility was demonstrated (by comparison to replicated glasshouse experiments) of producing LC omega3 in the field without any yield penalty (74). Thus, the choice of the oilseed crop Camelina as a host for the successful expression of the LC omega3 trait has been established.

8. Utility of Camelina LC Omega-3 Oil in Aquaculture The essential question must be; can the novel LC omega-3 oils generated in Camelina be used as a substitute for fish oil? To address this Betancor et al. (75) recently completed a study in which the EPA-containing Camelina oil described by Ruiz-Lopez et al. (72) was tested as a substitute for fish oil in a salmon feeding trial. In this study, fish oil (control), wild type (WT) and EPAcontaining Camelina oil (GM) were fed to juvenile Atlantic salmon within an iso-energetic diet for a period of seven weeks. At the end of the feeding trial all the fish had doubled in weight and displayed no indicators of ill health; moreover fatty acid analysis indicated the expected accumulation of EPA (as a

result of slow EPA conversion, levels of DHA in tissues were also shown to be increased). Further transcriptomic analysis produced a similar pattern of gene up regulation in fish receiving WT and GM Camelina oil; reflecting the fact that the GM Camelina oil is a modified vegetable oil and therefore contains a different chemical e.g. sterol composition to fish oil (75). As formulations for aquafeed diets are now composed of blended fatty acids from marine and vegetable sources, the Betancor study successfully demonstrated how LC omega-3 Camelina oil is appropriate for use in aquaculture.

9. Conclusion As discussed above there is a clear need within aquaculture for an alternative, sustainable supply of LC omega-3. The potential of engineered oilseed crops to meet this demand have been developed by a number of laboratories over the last fifteen years, but only now, at least with Camelina, has it been possible to demonstrate the viability of oilseed crops as a source of EPA and DHA. However, it is clear there are a number of hurdles before a Camelina LC omega-3 oil can become a commercial reality. It must be hoped that, subject to the appropriate regulatory and safety approvals, a forward looking aquafeed industry would be willing to adopt LC omega-3 Camelina oil in fish diets, thereby reducing the pressure on oceanic stocks. Camelina engineered to produce EPA and DHA, when grown in sufficient volume could make a significant contribution to reducing the demand from capture fisheries (200 000 ha of LC omega-3 Camelina could produce 150 000 Mt of oil or 15% of the global oceanic harvest) (65). The area required seems large, but it is in fact modest when placed in the context of global vegetable oil production. For example, such a hypothetical area would be less than 3% of the Canadian oilseed sowing area of a crop like canola (65). Of course before such numbers can be achieved on farms a number of issues must be resolved; crucially regulatory approval must be sought and obtained, the agronomy and breeding of Camelina must be addressed, oil formulations tested, and the views of consumers understood. All of these steps require significant effort and resolve, however the demand for LC

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scientific omega-3 is likely to grow, therefore it is our hope that this experimental terrestrial oilseed source of LC omega3 can be converted to a commercial reality.

Acknowledgments Rothamsted Research receives grantaided support from the Biotechnology and Biological Sciences research Council of the U.K. Some of the work described was supported by BBSRC grant BB/J00166X1.

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What is the future for oil palm as a global crop? Professor Denis J Murphy Head of Genomics and Computational Biology Research Group, University of South Wales, CF37 4AT, United Kingdom & Chair, Biology Advisory Committee, Malaysian Palm Oil Board, Bandar Baru Bangi, Selangor, Malaysia Email: denis.murphy@southwales.ac.uk Summary The African oil palm, Elaeis guineensis, is the major global vegetable oil crop. Palm oil is consumed daily by over two billion people and can be found in about half of all products on sale in a typical supermarket. Increased demand for palm oil, particularly in Asia and Europe, has led to extensive conversion of tropical habitats into plantations. In some parts of Southeast Asia, this has had adverse ecological and environmental consequences that have led to calls for boycotts of products containing palm oil. The industry is now responding to these pressures, albeit slowly and belatedly in some cases, and several schemes are in place to provide palm oil that is certified as being of sustainable origin. Advanced breeding methods, particularly genomics, are beginning to bear fruit in terms of crop improvement for yield, quality, and biologically based pest and disease resistance. In the future oil palm is set to become a truly global crop with important new centres of cultivation being developed in tropical Africa and the Americas. Key words palm oil, food, detergents, smallholders, plantations, peat soil, sustainability, advanced breeding, genomics, globalisation Abbreviations RSPO, Roundtable on Sustainable Palm Oil; HCS, High Carbon Stock; TILLING, TargetIng Local Lesions IN Genomes; CRISPR Clustered, Regularly Interspaced, Short Palindromic Repeats; TALENs Transcription Activator-Like Effector Nucleases; QTL, Quantitative Trait Loci

Introduction

alm oil is obtained from the fruits of the African oil palm, Elaeis guineensis. Oil palms originated in western Africa but are now grown in tropical regions around the world, most notably in Southeast Asia (see Table 1). The fleshy mesocarp of the palm fruits produces a vitamin-rich oil that is a basic foodstuff consumed on a daily basis by over two billion people (1). Palm oil is a particularly popular foodstuff in southern and eastern Asia where is it used for cooking and as a vegetable oil. Palm fruits are produced in large bunches that hang from the foliage near the tops of the trees and can be harvested year-round (see Figure 1). The major acyl components of palm mesocarp oil are oleic and palmitic acids, which makes it especially suitable for domestic and commercial cooking or frying applications. The oil is also ideal for the manufacture of solid or semi-solid products such as margarines, creams or chocolate-type confectionary items including drinks and spreads (2,3). For this reason, palm oil is used globally as an ingredient in numerous processed

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Figure 1. A relatively new commercial oil palm plantation on peatland in central Sarawak, Borneo.

foods and confectionary items, such as ice cream, biscuits, cakes, chocolate, pizzas as well as in a host of â&#x20AC;&#x2DC;ready mealâ&#x20AC;&#x2122; products. Indeed, it has been estimated that palm oil is present in as much as half of all products on sale in a typical supermarket (2). In addition to the edible oil from the fleshy mesocarp, the seeds, or kernels, of palm fruits contain a different type of oil that is enriched in medium-chain lauric and myristic fatty acids, which have many non-food uses. For

example, palm kernel oil provides the key functional constituents (i.e. lauric salts) in many cosmetics and cleaning products such as lipsticks, toothpaste, washing-up liquids, shower gels, shampoos, and laundry detergents to name but a few examples (1,2). Due to the ease with which medium chain fatty acids are absorbed by the body, palm kernel oil, which is similar in acyl composition to coconut oil, is also used in specialised edible applications including some hospital foods,

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Table 1 Major centres of oil palm production Source: United States Department of Agriculture, 2012

infant milk formula, and some sports nutrition products.

Why does palm oil have a poor reputation in some countries? Despite its evident importance for human nutrition, health and hygiene, the oil palm sector has been subject to increasing vilification in some parts of the world over the past decade. This had been mainly due to the perceived environmental and ecological impacts of some of the more recent oil palm plantations, especially in Indonesia, that have sometimes displaced pristine tropical habitats (4,5,6). There has also been a perception that palm oil has negative nutritional qualities, despite it being an important human food product for millennia. The poor perception of oil palm is hardly surprising because, over recent

years, much of the media coverage of oil palm has included bleak images of displaced orang utan and other wildlife (7) alongside burning, degraded tropical forests producing huge amounts of pollution and the release of greenhouse gases (8,9). This perception means that most people in the West have decidedly negative opinions about oil palm. In contrast, some groups in Asia have questioned the motives of certain antipalm NGOs, which they see as threatening a key aspect of economic growth in the region (10). The major criticism of the oil palm industry relates to the expansion of cultivation that has sometimes (but by no means always) been at the expense of rainforest. This expansion has been driven by increased demand for palm oil both in Asia and Europe. After 2000, increased global demand for food (mainly from India and China) and for biofuels and

Table 2 Major palm oil importers * India, Pakistan and Bangladesh; + Egypt, Iran, UAE, Turkey, Saudi Arabia, Iraq Source: United States Department of Agriculture, 2012

other non-food products (mainly from Europe) were the major factors behind the conversion of land in Southeast Asia (mostly in Indonesia) to oil palm cultivation (see Table 2). In Indonesia the area of oil palm cultivation more than trebled from 2.5 Mha (million hectares) to over 8 Mha between 2000 and 2014 (11). In some cases this has led to significant habitat loss for iconic species such as orang utan that has triggered large decreases in local populations (7). There have also been more general reductions in overall species biodiversity as complex ecosystems are replaced with simpler plantation systems that host fewer species (12). In some quarters, oil palm is now characterised as an evil that needs to be removed from the landscape. More recently there have been several well publicised anti-oil palm campaigns, especially in some Western countries. In certain cases these have involved the organisation of consumer boycotts of oil palm products ranging from cosmetics to chocolate (13,14,15). One example from June 2015, which involved an outspoken attack by the French minister of ecology, SĂŠgolĂ¨ne Royal on a company using palm oil, although this was subsequently fully retracted, as described in Box 1. In contrast to these negative views on oil palm, there is an increasing recognition that oil palm is a necessary crop that has many benefits, including supporting the livelihoods of millions of small farmers in Asia and Africa (17, 18). Rather than boycotting palm oil products, therefore, there is a movement to certify that such products are only obtained from plantations that can verify that their oil has been produced using sustainable methods and was not sourced from areas recently converted from sensitive forest or peatland habitats. The most important of these schemes is the Roundtable on Sustainable Palm Oil (RSPO) set up in the early 2000s) (19,20). It is important to realise, therefore, that in contrast to the highly critical views on oil palm often heard in the West, there is another perspective on oil palm that is much less frequently heard. This concerns an ancient and bountiful African tree crop whose fruits provide a wholesome, vitamin-rich oil that is an integral part of the diet of billions of people in 150 countries around the world (1). It is about a crop that is cultivated by a complex and wide ranging agricultural sector that ranges from

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scientific millions of smallholder farmers with tiny plots of a few dozen trees to less than a dozen very large multinational plantation companies each growing millions of trees. While there are undoubtedly examples of poor practice in this vast and diverse industry, serious efforts are now underway to meet modern targets for environmental impact and overall sustainability.

Box 1 – L’affaire Nutella: a minister is shamed On 15 June 2015, the French ecology minister, Ségolène Royal, metaphorically got Nutella on her face (see below) when she made an outspoken attack on the popular spread because it contains palm oil. As noted in the main text, Nutella only is one of many hundreds of palm-based food products and as many as half of all supermarket items include some palm oil. The minister was apparently unaware of this fact as she singled out Nutella during an interview on the French TV station, Canal+. But she then went further than just criticising Nutella and advised shoppers to boycott the spread so as to ‘sauver la planète’.

History of oil palm as a crop The African oil palm has been cultivated as a source of food and fibre by people in Western Africa for many thousands of years and was harvested by hunter gatherers for many millennia before then (21). Oil palm fruits were highly prized and were traded across the continent from the Atlantic coast to the Red Sea. For example, remnants of palm fruits have been found in vessels from an Egyptian First Dynasty tomb at Abydos dated to at least 5,000 years ago (22). Until recent times, cultivation remained mainly confined to the centre of crop origin in the West and Central African coastal belt between Guinea/Liberia and northern Angola. Additional cultivation is now found from 16° North in Senegal to 15° South in Angola, and eastwards to Zanzibar and Madagascar, but by far the best production levels are reached in the high rainfall areas between 7° North and South from the Equator (23). In the 19th century, oil palm was brought from Africa to Southeast Asia by Dutch and British colonists. It was originally brought to Java as an ornamental plant by the Dutch in 1848 but its economic potential was soon recognised. Seed selection in the Botanic Gardens of Singapore and Bogor and at the Deli Research Centre in Sumatra resulted in the development of commercial varieties of the crop that have been grown on an increasingly wide scale since the 1930s in what are now the nations of Malaysia and Indonesia. Large-scale oil palm cultivation was first commercialised by British planters in Malaya, during the mid-twentieth century. Following the fall in demand for natural rubber after the 1950s, many rubber plantations were converted to oil palm and much of the modern development of the crop has taken place in Malaysia since its independence in 1957 (23). In 2006, oil palm became the most important source of vegetable oil in the world (24). Today this former West

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Reaction from the food industry was swift with the minister being roundly condemned for her misinformed and intemperate attack on Nutella – and by extension a host of other foods. It was pointed out that Ferrero, the owner of the Nutella brand, sourced its palm oil from certified members of the Roundtable on Sustainable Palm Oil (RSPO). Just two days later the minister performed a volte-face and tweeted her apology thus:

‘L’affaire Nutella’ was amusing in the way it was reported in the Press. However, it also highlights the ignorance and prejudice concerning oil palm that even affects senior public figures that arguably ought to be better informed. In this case, it was very welcome that the minister had the grace to admit her mistake, but there are many other instances where misinformation has not been so promptly and publicly corrected.

African subsistence crop is a major export earner for Indonesia and Malaysia (23), which together account for 85% of total global production (see Table 1). One of the major factors driving this increased palm oil production is the seemingly insatiable demand to supply the expanding populations of India and China (1,24, Table 2). The 2.4 billion people in these two countries currently make up about 40% of the world population. In addition to their increasing populations, these two nations are

becoming more affluent and their higher standards of living are associated with increasing demands for vegetable oil (see Figure 2).

Oil palm is a uniquely productive product The current average annual yield of useful oil from an oil palm plantation in Malaysia is about 3.7 t ha-1 (tonnes per hectare). However, by improving the way the crop is managed and harvested, this yield can be almost doubled to over 6-7 t ha-1 on the more advanced

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scientific kernel oil (30). As noted below improved breeding and management have the potential over the next few years to produce >50% increase in oil yield as a conservative estimate (1). This would deliver an extra 35 Mt of edible oil available from the same area of land already in use for the crop, i.e. without the need to expand the area of cultivation. In contrast, the same amount of oil from major temperate oilseed crops, such as soybean or oilseed rape, would require cultivation of an additional 30-50 Mha of prime farmland in Europe or the Americas. This is 2-3 times the entire global area already occupied by oil palm plantations and such a vast area of land is simply unavailable in temperate regions.

Figure 2. Expected trends in world population and edible use of vegetable oil (taken from ref. 19).

commercial plantations (1). The greater yield on well-managed plantations is due to such measures as replanting with the latest genetically improved tree varieties, rigorously reducing crop losses from attacks by pests and diseases, optimising harvesting methods and minimising spoilage during transport and storage, and using the latest technology in processing mills. Even at current yields, on a per hectare basis, oil palm is 6-10 times more efficient at producing oil than comparable temperate oil crops such as rapeseed, soybean, olive and sunflower (1). In addition to its high oil yield, it is also a much more efficient crop than its competitors in terms of the intensity of land management, harvesting and processing required. For example, the annual oilseed crops require replanting each year, which involves regular disruption of the soil structure by ploughing. This means that in oil palm plantations the soil structure, or rhizosphere, has a rich organic content and is less disrupted compared to temperate oil crops. The temperate oilseed crops also require a brief but intensive annual period of harvesting and processing that often must be completed in a matter of days, whatever the weather. In contrast, an oil palm tree can be cultivated for 20-30 years without disturbing the soil. Another advantage of oil palm is that, within a given plantation, harvesting and processing can take place on a continual year-round basis within a

relatively predictable climatic regime that has far less seasonal fluctuation than in temperate regions. This means that the workforce, machinery, and other assets can be employed on a continuous basis throughout the year, rather than for a single intensive period, as is the case for annual oil crops (1). To draw an analogy with microbial biotechnology, oil palm husbandry resembles an efficient continuous culture system rather than the much less efficient batch-processing system represented by annual crop husbandry. As well as having a competitive edge over the annual oilseed crops, oil palm is also more productive than other oilbearing tree crops such as olive or coconut, which respectively yield oil at about 2.0 t ha-1 and 0.3 t ha-1. Given that the annually cultivated oilseed crops grown in western countries only produce oil in the range of 0.5-1.5 t ha-1, it is clear that oil palm has significant potential, not only to satisfy the increasingly demanding markets for edible oil in India and China, but also to act as a source of valuable non-food products for the global oleochemicals industry. In addition, although the use of food crops for biodiesel has been rightly criticised (25-28), if it is really necessary to produce biodiesel in the short term, oil palm is by far the most efficient and least land-consuming crop that can be used (28,29). The total global production of palm oil in 2015 is estimated at about 72.6 Mt, made up of 65.2 Mt mesocarp oil and 7.4 Mt

Oil palm is grown both by smallholders and by large plantation companies A common misconception about oil palm is that it is overwhelmingly a â&#x20AC;&#x2DC;big businessâ&#x20AC;&#x2122; crop. In fact, there are more than 3 million smallholders growing the crop, nearly all of whom farm individual familyowned plots. In Indonesia, which is the largest oil palm producing country, smallholder plots account for 40% of the total crop area (31,32). In terms of international trade, the medium to large commercial plantations are the dominant players and it is this sector that has been most active in joining RSPO or similar certification schemes. However, the smallholder sector has played a vital role in the economic advancement of millions of relatively poor rural people who have been able to purchase modern goods and educate their children (see Figure 3). Smallholders also have millions of votes and are therefore an important constituency in rural areas of Malaysia and Indonesia that governments ignore at their peril. Unfortunately, most smallholders do not have the resources or economies of scale to match larger plantations and their crops are in general less efficiently managed with yields lower than the national average (33). Another serious issue for smallholders throughout Southeast Asia is that they are either unaware and/or cannot afford to join sustainability certification schemes such as RSPO (34). In general, most smallholders in the past have not had access to some of the best elite germplasm developed by commercial companies, and in many

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scientific Such a scheme, which would have a guaranteed bonus in generating higher oil yields, could also reduce future pressures to convert pristine habitats to oil palm plantations. Failure to implement oil palm replanting will mean declining yields in the coming decade and, given the likelihood of continuing international demand for palm oil, impoverished smallholders might decide to embark on a new round of ecologically undesirable land conversion.

Role of Sustainable Palm Oil plantations

Figure 3. These elderly smallholders farm a 3.2-hectare plot in Sarawak. Their farm includes about 500 oil palm trees intercropped with pineapples that provide their family with the income that has enabled them to educate their children and grandchildren. The average age of a smallholder in Malaysia is now over 55 but they still typically play important roles in supporting several younger generations of the family.

cases they simply buy uncertified seed from local merchants. The decision on whether or not to replant new trees is problematic for smallholders as it means losing their income for as much as 5 years until the new trees produce fruit. It is another 5 years before a good level of productivity is reached but these mature trees will then maintain good yields for two further decades before a decline sets in. Many trees on smallholder plots are now well beyond their productive lifetime and are giving steadily decreasing yields. National replanting schemes are therefore needed for the sake of the smallholders and the efficiency of the sector as a whole. The Malaysian government is now addressing this problem by committing US$135 million to facilitate a national replanting programme that is particularly targeted at smallholders (35). The government has estimated that 365,000 ha of mainly smallholder oil palms are 25-37 years old, which means that they are well beyond their normal productive lifetime. The aim is to replace 100,000 ha of ageing oil palms per year by providing grants to smallholders for the replanting costs plus an annual allowance for the first two years of zero productivity. It is hoped that the larger commercial plantations will also replant a further 100,000 ha yr-1 so that by 2018, over 1 Mha will have been replanted. If this can be achieved, and with the assumption that new oil palms capable of 5-6

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t ha-1 will be planted to replace the current ageing stock producing 2-3 t ha-1, this rate of replanting could result in an additional oil yield in the region of 3 Mt in Malaysia by 2020 (1). This >10% increase in yield can be readily achieved without converting any new land to oil palm and by using currently available plant varieties. In reality, as discussed below, much higher yielding varieties will soon be available from ongoing breeding programmes, so there is even greater potential to increase Malaysia palm oil yields in the coming years. The replanting issue that is currently such an urgent problem in Malaysia will also eventually affect Indonesia, which is an even larger palm oil producer. Many plantations in Indonesia were installed during a comparatively brief period about two decades ago, meaning that most of them will require replacement, and consequent loss of income for growers, at about the same time. The situation in Indonesia will be exacerbated by the far larger proportion of oil palm cultivated by smallholders compared to Malaysia. It is estimated that over the next decade as much as 500,000 ha yr-1 will require replanting in Indonesia (1). It would therefore be prudent for the Indonesian government to use some of the considerable revenues it is now receiving from a buoyant palm oil market to set aside funds for a largescale national replanting programme in the early 2020s.

Over the past year or so the pendulum of informed opinion has started to swing away from a simplistic view of oil palm as being an unmitigated environmental scourge (see Box 1). Instead a more nuanced approach is gradually emerging that recognises the genuine pros and cons of this bountiful tropical crop. One of the most encouraging developments has been the establishment of RSPO as a robust and independent body to certify the environmental and social credentials of palm oil. The RSPO vision is â&#x20AC;&#x153;transform the markets by making sustainable palm oil the normâ&#x20AC;?. As of mid-2015 the RSPO had over 2,000 members globally that represent 40% of the palm oil industry, covering all sectors of the global commodity supply chain. An estimated 11.75 Mt of global palm oil is currently certified by RSPO and the total is increasing steadily by the year. The RSPO scheme is by no means perfect, as pointed out by some NGOs (36), but more recently the scheme has been praised by other NGOs for its firm action in expelling members that do not conform to standards (37). Unfortunately, some companies have ignored the scheme altogether, often citing high costs and the difficulties of maintaining and checking identity preservation of RSPO-certified batches of oil in what has hitherto been a commodity product. The development of traceability methods and reliable assays of batch origin are important challenges in order to enable quality assurance of certified oil cargoes. As we saw above, few smallholders can afford RSPO certification and this has led to the establishment of other schemes with lower thresholds, such as MSPO (38) or ISPO (39) in Malaysia and Indonesia respectively. While these schemes have their merits in engaging producers, especially smallholders, who feel unable to qualify for RSPO (40), they run the risk of being regarded by

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scientific some NGOs, palm oil users and consumers as being a sort of ‘RSPOlite’ (41). For this reason, the majority of large European palm oil importing companies, such as Nestle, Unilever, Ferrero, Loders Croklaan, plus many major plantation companies, such as Sime Darby, IOI and United Plantations, have already signed up to RSPO. The UK government has set an ambitious goal of having 100% of edible palm oil imports as RSPO certified by the end of 2015. To quote from a governmentcommissioned report: “Many major UK and international businesses that use or sell palm oil have made commitments to 100% sourcing of sustainable palm oil by a given deadline, generally 2015.” (42). Similar commitments have been made by the governments of Belgium and the Netherlands (20). Most people would agree that, whatever its limitations, RSPO probably represents the best vehicle currently available for the sustainability of palm oil. This is especially true for large-scale producers and major users in the food and cosmetics industries, where their consumers can be sensitive to the eco-environmental credentials of such products. For example, while one cosmetics retailer (Lush) has boycotted palm oil (resulting in considerable problems in sourcing alternatives), another retailer (Body Shop) has used 100% RSPO certified palm oil since 2011.

Assessing environmental impact and sustainability One of the most important limitations in developing robust policies for a sustainable and environmentally sound oil palm industry is a lack of hard facts about the precise eco-social impacts of palm oil production and utilisation from ‘cradle to grave’. As an example, the following quote is from a 2015 study on ecosystem services provided by oil palm plantations: “Our review highlights numerous research gaps. In particular, there are significant gaps with respect to information functions (socio-cultural functions). There is a need for empirical data on the importance of spatial and temporal scales, such as the differences between plantations in different environments, of different sizes, and of different ages. Finally, more research is needed on developing management practices that can off-set the losses of ecosystem functions.” (43).

Scientific studies of the environmental and socio-economic impacts of oil palm are in their infancy and are fraught with problems due to the huge breadth, complexity, and interdisciplinary nature of the systems involved. These already formidable challenges can be exacerbated by the roles of vested interests from all sides of the debate who will often cherry pick partial data from selected studies in order to back their already entrenched views. In order to be credible, therefore, studies on oil palm sustainability should be performed by independent researchers and the results published in full, preferably in peer reviewed international scientific journals. Moreover, such studies should not only focus on oil palm, but should carry out similar assessments of other oil crops in order to compile a comparative balance sheet of the various plus and minus points of other cropping systems, e.g. soybean or rapeseed, in the context of impact and sustainability. One of the major tools for such a process that is much used by policymakers is life cycle assessment (LCA). This method seeks to estimate the impact of all aspects of the production process from planting seed, growing, harvesting and processing the crop (including fuel and labour costs); application of inputs such as water, fertiliser, herbicides, pesticides etc; shipping of the oil overseas and its downstream conversion into other products including foods and oleochemicals; transport to wholesalers, retailers, and consumers; and finally disposal of all products at the end of their lifetimes. These are only a few of the dozens of parameters involved in a comprehensive LCA and very few published studies manage to cover the entire system. Despite these caveats and limitations, some useful LCA data are now emerging where oil palm is compared with some of the other major oil crops. An example is a 2015 study, which shows that overall impact of oil palm, as determined by LCA methods, is comparable, and sometimes superior to the temperate crops (44). Many more such studies are needed in order to inform better public debate and future policy about the true environmental impacts of oil crops.

Ecological and climaterelated studies During the past few years there has been a welcome increase in research

Figure 4. Dr Selliah Paramananthan analysing peat soil composition in an oil palm plantation in Borneo. New analyses of different types of peat soils should inform decisions about whether or not particular soils are suitable for oil palm cultivation (see main text).

on the comparative ecology of oil palm plantations, the impacts of land-use change, and the possible effects in relation to climate change, including a balance sheet for greenhouse gas emissions during conversion of forest or peatland to plantations. There is insufficient space here to discuss all of these studies but a few examples will now be outlined. The High Carbon Stock (HCS) Science Study was set up by five major oil palm growers (Asian Agri, IOI Corporation Berhad, Kuala Lumpur Kepong Berhad, Musim Mas Group, and Sime Darby Plantation), together with Cargill and Unilever, to increase their commitment to sustainable palm oil (45). This group, which is jointly chaired by the academic, John Raison, and wellknown environmentalist, Jonathon Porrritt, issued a draft report for discussion in 2015, in which they produce values for various environmental impacts and list a series of recommendations for future conduct of the industry (46). Two other recent studies examine the potential impact of land use and climate change on biodiversity in Borneo where a great deal of oil palm planting has occurred (47,48). The conclusions include the need to establish nature reserves in upland areas where climate change will be less severe and also to improve connections between reserves and

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Figure 5. A deformed oil palm tree growing on waterlogged peatland in Borneo. As noted in ref. 56, there are several types of peatland with different levels of organic materials. A lower organic content may mean the peat is suitable for palm cultivation while higher organic contents tend to be unsuitable.

plantations via wildlife corridors. One of the most controversial aspects of new palm cultivation is the use of tropical peatland, especially in Borneo. There are several ongoing studies of the impact of peatland conversion in terms of greenhouse gas emissions (49-55). However, more studies by independent groups will be necessary in order to generate sufficient data for a meta-analysis that could provide robust policy options for the exploitation (or not) of peat soils. Other studies, including a systematic analysis of tropical peat soils (56), have demonstrated an unexpectedly complex picture with several different

categories of peat (see Figure 4), some of which can readily support oil palm crops while other types cannot (see Figure 5). The conclusion is that it is not appropriate to impose blanket bans on the use of peat soils for oil palm cultivation but rather to survey the soil first before making a better informed decision (see Figure 6).

Investing in modern breeding and crop management Plant breeding is a cornerstone of crop improvement, as shown by the Green Revolution of the 1960s and 1970s

Figure 6. Peatland in Borneo being drained in mid-2015 prior to planting oil palm. This area is mostly secondary woodland that had been logged over many years previously.

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that successfully averted the spectre of famine in many developing countries (57). During the 1980s and 1990s, advanced breeding methods, such as hybrid creation, assisted crosses and introgression of wild germplasm, were instrumental in enabling rice yield to increase five-fold in some regions of Asia. During the 2000s, much attention has been focussed on genomic approaches to plant breeding with the deployment of a new generation of technologies, such as DNA marker-assisted selection, genome sequencing, transgenesis (genetic engineering or GM) and automatic mutagenesis/selection (TILLING, TargetIng Local Lesions IN Genomes) (57). More recently new genome editing technologies such as the CRISPR (Clustered, Regularly Interspaced, Short Palindromic Repeats) and TALENs (Transcription Activator-Like Effector Nucleases) are showing even more promise for crop and livestock improvement (58-61). In 2015, the CRISPR/Cas9 system was described in a Nature article as “the biggest game changer to hit biology since PCR” (62). All of the above methods have considerable potential for oil palm improvement and one of the most encouraging features of recent years is the development of systems to underpin future breeding efforts. A key achievement has been the development of genomics and related ‘omic technologies by oil palm researchers (1). These efforts culminated in July 2013 when the journal Nature published two back-to-back papers that described the sequencing of the genomes of two related oil palm species, E. guineensis and E. oleifera plus the associated discovery of the Shell gene that regulates fruit thickness (63,64). Thin shelled fruits, as found in tenera hybrids, are high oil yielding and are now the basis for all commercial oil palm production in South-east Asia. Identification of the Shell gene will enable breeders to use molecular markers to select suitable breeding lines, instead of waiting three to four years or more for the young plants to produce fruits for selection via a visual phenotype. This notable achievement was followed in September 2015 by a further Nature paper reporting the identification of the epigenetic mechanisms that underlie the serious ‘mantling’ problem that has bedevilled efforts to use clonal propagation in the

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scientific industry (65). As with some other tree crops, tissue culture and micropropagation are often the best way to produce thousands or even millions of clonal copies of selected elite individuals. Unfortunately, in the case of oil palm, epigenetic abnormalities regularly arise during tissue culture but it can take several years before the resultant deformed or ‘mantled’ fruits can be observed. This has cost the industry millions of dollars and much wasted time in growing useless trees. The elucidation of the ‘mantled’ trait will allow for much earlier detection and elimination of affected trees and will therefore contribute to raising overall oil yield in the industry (66). Oil palm breeders are also using advanced selection methods, including genetic markers based on DNA sequences, to assist in the selection of favourable agronomic traits. Other modern techniques like association genetics and quantitative trait loci (QTL) analysis are also enabling chromosomal regions and individual genes involved in the regulation of important traits to be mapped and identified (57). These methods have recently been used to map the lipase gene involved in oil deterioration in ripe palm fruits (67) and QTL analysis of genes regulating the fatty acid composition of palm oil (68). Bioinformatic and ‘omics methods are being used to annotate the oil palm genome and to discover genes

for premium edible markets and as feedstocks for medium-value oleochemicals such as lubricating oils (1).

The future of oil palm in Southeast Asia

Figure 7. Mature oil palm trees can reach over 20 metres in height, which makes it difficult and costly to harvest the fruits. Semi dwarf trees use less energy in making a tall trunk and can produce higher fruit yields. They are also much easier to harvest mechanically.

involved in the regulation of key traits such as oil yield and quality, semidwarf trees and pest/disease resistance (69-72) (see Figures 7 & 8). Efforts are also underway to breed high-oleic varieties of oil palm. These varieties could compete with oilseeds, such as sunflower and rapeseed, both

Figure 8. The most important pathogen of oil palm is the fungus, Ganoderma boninense, which forms fruiting bodies around the base of infected trees and eventually kills them. Genomic methods are now being developed to combat this disease, which affects 30-50% of oil palms in some parts of Indonesia and

Although, it should be possible to produce a lot more palm oil by increasing the crop yield, it seems inevitable that, at least in the shortterm, some additional land conversion will be necessary (1). There are several drivers for the continued expansion of demand for palm oil in the medium to long-term future, the most important of which population growth and economic progress in many developing countries. In 2015, a global area of about 16 Mha produced 72.6 Mt of palm mesocarp + kernel oils. Forecasting future levels of demand for any commodity is always challenging, but the following estimates from several reliable sources predict that about 77 Mt palm oil will be required by 2018 (73); 84 Mt by 2020 (74); and between 93 and 156 Mt by 2050 (19). This is a formidable challenge but one that is achievable by a judicious mixture of management improvements, replanting better genetic stock, and some expansion of cultivation into other parts of the tropics. Providing any new cultivation is carried out in an environmentally responsible manner, there are benefits from diversifying oil palm cultivation into other regions of the world. For example, a more dispersed cropping area will be more resilient to threats from climatic factors or locally adapted pests and pathogens. In this respect, the current concentration of >85% of global palm cultivation in one geographical area Malaysia/Indonesia) is far from ideal. The expansion of cultivation into suitable areas of West Africa and South/Central America that is now underway will create a more secure production system in the longer term. It is also worth pointing out that, as shown in Figure 9, none of these regions comes close matching to the cropping intensities already adopted in large parts of the USA and Europe. Some of these measures could have a significant impact on output within the next five years. For example, if the planned replanting programme in Malaysia (see above) is carried out, it could deliver an additional annual yield of 5 Mt palm oil on existing land. If some of the best existing experimental

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Figure 9. Proportion of cropland around the world. Note that by far the most intensively cropped areas are found in Europe, North America, and the Indian Subcontinent. In contrast, Southeast Asia has more moderate crop levels (84).

breeding material, theoretically yielding 8-10 t ha-1, could be developed for commercial planting throughout the sector then yield could be increased by 50% or more. This could deliver as much as 30 Mt more oil per year â&#x20AC;&#x201C; again without requiring further land conversion. Further into the future, there is the prospect of additional yield gains by using modern breeding technologies to produce fruits with a higher oil content and dwarf oil palms that bear more fruit and are easier to harvest mechanically. At present, we cannot quantify the benefits of such biological innovations but they could potentially deliver tens of millions of tonnes of additional oil.

The future of oil palm in Africa and the Americas In recent years there has been significant expansion of oil palm cultivation in Africa and the Americas. Currently, the three major centres of cultivation in Central/South America are Colombia, Ecuador and Honduras with a modest annual output of 2 Mt oil. According to IIASA estimates, these three countries and Peru have some potential to expand cultivation but by far the largest new prospective area is in Brazil. Oil palm is more suitable as a crop in low elevation regions in the humid tropics and can even tolerate the highly acidic non-forest soils of Amazonia (75). In Brazil, an estimated 32 Mha (excluding rainforest) are suitable for oil palm production (76), which is double the entire global oil palm area at present. It should be stressed that the vast majority of this

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possible expansion into oil palm in South America would be on grassland or planted pasture with very little, if any, forest conversion (77). Conversion of such land would therefore have a lower impact on biodiversity and other sensitive environmental indicators that the conversion of tropical forest. West Africa is the historical home of the commercial oil palm and, prior to the 1960s, Nigeria was a globally dominant producer. Since then, civil conflict plus poor investment and management of the largely smallholder dominated industry led to a sharp decline in palm oil production. By 2000, Nigeria was unable even to meet local demand and the country is now a net importer of edible oils (78). However, the buoyant international demand for palm oil is stimulating the replanting of disused plantations or establishment of new plantations in several parts of West and Central Africa (79). Much of this expansion will be required just to meet local requirements for vegetable oil. For example, in 2010, Africa imported 2.4 Mt palm oil, mostly from Malaysia. It is estimated that 24 Mha is suitable for growing oil palm in Nigeria alone (80). In terms of climate and agronomy, another promising region for new oil palm cultivation in Africa is in the Congo River basin (81) and plantation companies are also steadily acquiring land in this and other parts of Africa (82).

Conclusions The oil palm industry faces many

challenges in the future. However, the tools to surmount these challenges already exist and have the potential to further transform this historic crop into a truly global source of nutritious food and valuable nonfood products for the growing world population. Higher yielding cultivars with improved oil compositions and greater resistance to pests and diseases will be available. We can also look forward to an extension of oil palm cultivation in new areas of the tropics. Over the next decade, West and Central Africa will begin to emerge alongside Central/ South America as major producers of palm oil, initially for local consumption but eventually for export to global markets. Between them, West/Central Africa and Central/South America have the capacity to convert well over 30-40 Mha to oil palm with a current yield potential of 130- 170 Mt oil, and much more than that if the expected increases in crop yields are realised. It is highly unlikely that such a vast area, which is more than double the present oil palm area, will need to be converted. However, even if only a quarter of this land is changed to oil palm plantations, these regions could be producing as much as 50-60 Mt oil by 2025. This is close to the present global total and demonstrates that a doubling of palm oil production in the next few decades is quite feasible. A redesign of plant architecture, especially the breeding of shorter stem, can further increase yields as well as transforming the management and processing of the crop. If these and other genetic improvements and

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scientific management efficiencies can be achieved, the resulting increased palm oil output could more than meet even the highest projections for future vegetable oil requirements. Moreover, given its superior yield and land-use efficiency, oil palm might eventually displace some of the less efficient temperate oilseed crops as the preferred source of oil for many edible and non-edible markets.

Policy Proposals The oil palm industry faces many challenges regarding its environmental credentials. These challenges are common to all regions and companies with little differentiation among the general public between ‘good’ and ‘bad’ sources of palm oil. Therefore the entire sector tends to be stigmatised by poor practice in a few areas. It is highly desirable that this huge global industry, which is worth over US$50 billion annually, should collectively redouble its efforts to address sustainability and public image issues as a matter of priority. One way to meet such challenges would be to form a global industry-wide body to facilitate best practice. The remit of such a body could include: Sponsoring independent research across the various disciplines related to the sector. Specific R&D areas might include yield and oil quality, pest/ disease resistance, addressing management-related issues such as ecological and environmental impact, product image, tree replanting, labour supply and mechanisation. Engaging independent experts in order to improve communications with NGOs and engage more effectively in a constructive dialogue with the general public. Development of robust methods to validate sustainably certified palm oil. As certified palm oil (e.g. via RSPO) becomes increasingly common it will be necessary to validate the provenance of such oil in order to reassure end users, including household consumers. The development of reliable traceability protocols and verification methods for batch origin (as already done for olive oil) are important challenges in order to enable quality assurance of certified palm oil cargoes.

References 1. Murphy DJ (2014) The future of oil palm as a major global crop: opportunities and challenges, Journal of Oil Palm Research, 26, 1-24

2. Gunstone FD (2011) Supplies of vegetable oils for non-food purposes, European Journal of Lipid Science and Technology 113, 3-7 3. Gunstone FD, Harwood JL, Dijkstra AJ eds (2007) The Lipid Handbook, CRC Press, Boca Raton, Florida 4. Brown E and Jacobson MF (2005) Cruel Oil, how palm oil harms rainforest & wildlife, Center for Science in the Public Interest, Washington, DC 5. May-Tobin C et al (2012) Recipes for success, solutions for deforestation-free vegetable oils, Union of Concerned Scientists, Boston, available online: www.ucsusa.org/deforestationfree 6. Gaveau DLA et al (2014) Four Decades of Forest Persistence, Clearance and Logging on Borneo, PLOS one 9, e101654 7. Wich D et al (2012) Understanding the Impacts of Land-Use Policies on a Threatened Species: Is There a Future for the Bornean Orang-utan? PLOS one 7, e49142 8. Carlson KM et al (2012) Carbon emissions from forest conversion by Kalimantan oil palm plantations, Nature Climate Change, 3, 283-287 9. Carlson KM et al (2012) Committed carbon emissions, deforestation, and community land conversion from oil palm plantation expansion in West Kalimantan, Indonesia, Proceedings of the National Academy of Sciences USA 109, 7559-7564 10. Khor YL (2011) The oil palm industry bows to NGO campaigns, Lipid Technology 23, 102-104 11. USDA (2013) Commodity Intelligence Report INDONESIA: Palm Oil Expansion Unaffected by Forest Moratorium http://www.pecad.fas.usda.gov /highlights/2013/06/indonesia/ 12. Barcelos E et al (2015) Oil palm natural diversity and the potential for yield improvement, Frontiers In Plant Science 6:190 13. UK boycott (http://www.saynotopalmoil.com) 14. France boycott (https://www.change.org /p/au-gouvernement-français-interdire-l-huile-depalme-et-ses-dérivés-dans-tout-produit-vendu-enfrance-2) 15. Italian boycott http://www.foodnavigator.com /Policy/Petition-to-limit-palm-oil-attracts-morethan-50-000-signatures 16. Roundtable on Sustainable Palm Oil (2015) Impacts website: http://www.rspo.org/ about/impacts 17. Basiron Y (2007) Palm oil production through sustainable plantations, European Journal of Lipid Science and Technology 109, 289–295 18. Sargeant HJ (2001) Oil Palm Agriculture in the Wetlands of Sumatra: Destruction or Development? European Union Ministry of Forestry, Brussels 19. Corley RHV (2009) How much palm oil do we need? Environmental Science and Policy 12, 134139 20. Balch O (2013) Sustainable palm oil: how successful is RSPO certification? Guardian, 4 July 2013, available online: http://www.theguardian.com/sustainablebusiness/sustainable-palm-oil-successful-rspocertification 21. D’Andrea AC, Logan AL and Wilson DJ (2006) Oil palm and prehistoric subsistence in tropical West Africa, Journal of African Archaeology 4, 195222 22. Fridel MC (1897) Sur les matieres grasses trouvees dans des tombes egyptiennes d’Abydos, Comptes Rendu 24, 648-651 23. Corley RHV, Tinker PB (2003) The Oil Palm, 4th edition, Blackwell, Oxford, UK 24. Murphy DJ (2007) Future prospects for oil palm in the 21st century: Biological and related challenges, Eur. J. Lipid Sci. Technol. 109, 296-306 25. Bringezu, S. et al. (2009) Assessing biofuels: towards sustainable production and use of resources, United Nations Environment Programme, Paris, France, available online: www.unep.org 26. Johnston M et al. (2009) Resetting global

expectations from biofuels, Environmental Research Letters 4, 014004 27. Van Noorden R (2013) EU debates U-turn on biofuels policy. Key vote could signal withdrawal of support from biodiesel, Nature 499, 13-14 28. Murphy DJ (2012) Oil crops: a potential source of biofuel, In: Technological Innovations in Major World Oil Crops, Volume 2, Springer, Berlin, pp 269-284 29. Long SP et al (2015) Feedstocks for Biofuels and Bioenergy, pp 302-347 In Scope Bioenergy & Sustainability: Bridging the Gaps, Souza GM et al, eds, SCOPE, São Paulo 30. Global Palm Oil Production, September 2015, available online: http://www.globalpalmoilproduction.com 31. Euler M, Schwarze S, Siregar H, Qaim M (2015) Oil palm expansion among smallholder farmers in Sumatra, Indonesia, EFForTS discussion paper series 8, available online: http://resolver.sub.unigoettingen.de/purl/?webdoc-3946 32. Edwards RB (2015) Palm oil and poverty in Indonesia, American Economic Journal: Applied Economics, under review, available online: https://crawford.anu.edu.au/files/uploads/crawfor d01_cap_anu_edu_au/201508/edwards_palm_oil_jmp_for_web.pdf 33. Abdullah R (2013) Technical Efficiency of Independent Oil Palm Smallholders (ISH) in Peninsular Malaysia with Respect to Fertiliser and Land Size, Oil Palm Industry Economic Journal 13, 27-37 34. ZSL (2013) New Britain Oil Palm: Smallholder. Overcoming Challenges in Certifying Smallholders, ZSL website: http://www.sustainablepalmoil.org/growersmillers/growers/case-studies/new-britain-palm-oil 35. USDA (2012) Malaysia: Stagnating palm oil yields impede growth, Commodity Intelligence Report, Dec 2012, http://www.pecad.fas.usda.gov /highlights/2012/12/Malaysia/ 36. Greenpeace (2013) Palm Oil, available online: http://www.greenpeace.org.uk/forests/palm-oil 37. Sustainable Brands (2015) RSPO Cleans House of Companies Failing to Meet Standards; NGOs Applaud, available online: http://www.sustainablebrands.com/news_and_vie ws/organizational_change/sustainable_brands/rsp o_cleans_house_companies_failing_meet_sta 38. Malaysian Palm Oil Council (2014) For a Better, More Responsible Certification on Palm Oil, available online: http://www.mpoc.org.my/ For_a_Better,_More_Responsible_Certification_on_ Palm_Oil.aspx#sthash.DL4iE1y0.dpuf 39. Indonesian Sustainable Palm Oil (ISPO) website: http://www.sustainablepalmoil.org/ standards-certfication/certificationschemes/indonesian-sustainable-palm-oil-ispo/ 40. Danielson M (2015) More Malaysian oil palm farmers to get MSPO certification, Palm Oil Health, available online: http://www.palmoilhealth.org /news/more-malaysian-oil-palm-farmers-to-getmspo-certification/ 41. Malaysian Palm Oil Scheme: more problems, fewer answers, Rainforest Action Network, available online: http://www.ran.org/tags/rspo?page=2 42. Proforest (2011) Review of policy options relating to sustainable palm oil procurement EV0459, Final Report to the Department for Environment, Food and Rural Affairs, DEFRA, London 43. Dislich C et al. (2015) Ecosystem functions of oil palm plantations - a review, EFForTS discussion paper 16, http://webdoc.sub.gwdg.de/pub /mon/sfb990/dp-16.pdf 44. Schmidt JH (2015) Life cycle assessment of five vegetable oils, Journal of Cleaner Production 87, 130-138 45. Full details of the High Carbon Stock Science Study and its governance arrangements can be found at www.carbonstockstudy.com)

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scientific 46. Raison J et al (2015) HCS (High Carbon Stock) Science Study: Draft Synthesis Report, Sustainable Palm Oil Manifesto, Sime Darby, Malaysia: available online www.hcsstudy.secretariat @simedarby.com 47. Scriven SA, Hodgson JA, McClean CJ, Hill JK (2015) Protected areas in Borneo may fail to conserve tropical forest biodiversity under climate change, Biological Conservation 184, 414-423 48. Struebig MJ et al (2015) Targeted Conservation to Safeguard a Biodiversity Hotspot from Climate and Land-Cover Change, Current Biology 25, 372-378 49. Chase L et al (2012) PalmGHG. A Greenhouse Gas Accounting Tool for Palm, available online: http://www.rspo.org/publications/download/059d 9f773ec950c 50. Agus F, Gunarso P, Sahardjo, BH, Harris N, Noordwijk M, Killeen TJ (2013) Historical CO2 Emissions from Land Use and Land Use Change from the Oil Palm Industry In Indonesia, Malaysia And Papua New Guinea, (pp 65-87) In Reports from the Technical Panels of the 2nd Greenhouse Gas Working Group of the Roundtable on Sustainable Palm Oil (RSPO). 51. Dalal R (2015) Consulting Study 6: Practical guidance on how to estimate soil carbon stocks and greenhouse gas emissions following tropical forest conversion on mineral soil 52. Gunarso P, Hartoyo ME, Agus F, Killeen TJ (2013) Oil Palm and Land Use Change In Indonesia, Malaysia And Papua New Guinea. (pp 29-63) In Reports from the Technical Panels of the 2nd Greenhouse Gas Working Group of the Roundtable on Sustainable Palm Oil (RSPO) 53. Lawson IT et al (2014). Improving estimates of tropical peatland area, carbon storage, and greenhouse gas fluxes, Wetlands Ecology and Management 23, 327-346 54. Khoon KL, Cobb A, Harun MH (2012) The Potential of Oil Palm in the global Carbon Cycle, Palm Oil Developments 54, 8-18 55. Khoon KL, Jepsen MR (2015) Carbon stock of oil palm plantations and tropical forests in Malaysia: A review: Carbon stock of Malaysian forest and oil palm, Singapore Journal of Tropical Geography 36, 249-266 56. Veloo R, Paramananthan S, Van Ranst E (2014) Classification of tropical lowland peats revisited: The case of Sarawak, Catena 118, 179-185 57. Murphy DJ (2011b) Plants, Biotechnology, and Agriculture, CABI Press, UK 58. Hsu PD, Lander ES, Zhang F (2014) Development and applications of CRISPR-Cas9 for

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genome engineering, Cell 157, 1262-1278 59. Belhaj K, Chaparro-Garcia A, Kamoun S, Patron NJ, Nekrasov V (2015) Editing plant genomes with CRISPR/Cas9, Current Opinion in Biotechnology 32, 76–84 60. Zhang H et al. The CRISPR/Cas9 system produces specific and homozygous targeted gene editing in rice in one generation. Plant Biotechnol Journal 2014, 12:797-807 61. Laible G, Wei J, Wagner S (2015) Improving livestock for agriculture – technological progress from random transgenesis to precision genome editing heralds a new era, Biotechnology Journal 10, 109-120 62. Ledford H (2015) CRISPR, the disruptor, Nature 522, 20-24 63. Singh R et al (2013a) Oil palm genome sequence reveals divergence of interfertile species in Old and New worlds, Nature 500, 335-339 64. Singh R et al (2013b) The Shell gene of the oil palm (Elaeis guineensis) controls oil yield and encodes a homologue of SEEDSTICK, Nature 500, 340-344 65. Ong-Abdullah M et al (2015) Loss of Karma transposon methylation underlies the mantled somaclonal variant of oil palm, Nature, advanced online publication, doi:10.1038/nature15365 66. Paszkowski J (2015) The karma of oil palms, Nature, advanced online publication, doi:10.1038/nature15216 67. Morcillo F et al (2013) Improving palm oil quality through identification and mapping of the lipase gene causing oil deterioration, Nature Comm 4:2160 68. Montoya C et al (2013) Quantitative trait loci (QTLs) analysis of palm oil fatty acid composition in an interspecific pseudo-backcross from Elaeis oleifera Cortés and oil palm (Elaeis guineensis Jacq.), Tree Genetics & Genomes 9, 1207-1225 69. Singh R et al (2009) Mapping quantitative trait loci (QTLs) for fatty acid composition in an interspecific cross of oil palm, BMC Plant Biology 9,114 70. Ting N-C et al (2013) Identification of QTLs associated with callogenesis and embryogenesis in oil palm using genetic linkage maps improved with SSR markers. PLoS ONE 8: e53076 71. Pootakham W et al (2013) Development and characterization of single-nucleotide polymorphism markers from 454 transcriptome sequences in oil palm (Elaeis guineensis), Plant Breeding 132, 711-717 72. Rosli et al (2015) Identification Of Candidate Genes Associated With Disease Resistance Related

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instructions

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his international Journal publishes articles based upon scientifically derived evidence that addresses problems and issues confronting world agriculture and food supplies. Articles will be subject to review by two or more scrutineers before acceptance. Authors are encouraged to take a critical approach to world-wide issues and to advance new concepts. Those wishing to submit an unsolicited article should in the first instance send a short summary of their intended paper in English by electronic mail to the Editor. The journal will publish suitable articles on agriculture and horticulture and their climatic, ecological, economic and social interactions. Relevant aspects of forestry and fisheries as well as food storage and distribution will also be acceptable. The Journal is not available for communication of previously unpublished experimental work, although original deductions from existing information are welcome. Statements must be based on sound scientifically derived evidence and all arguments must be rational and logically derived. Typical articles will be between 1 000 and 3 000 words, with photographs, and figures, line drawings and tables, where relevant. Articles outside these lengths may be acceptable, if the length can be justified. Articles that pose questions and raise issues for which answers are needed will be accepted if they meet the necessary criteria. Such questions may for example, describe an economic or husbandry problem in a developing country or ocean, resulting from climate change or some unintended consequence of policy, for which no clear solution is at hand. World Agriculture will produce one volume each year with Issue numbers 1 and 2 occurring within each volume. Page numbers will run consecutively throughout each volume from page one onwards.

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