World agriculture vol 4 no 2 by Script Media

editors World Agriculture Editorial Board Patron Sir Crispin Tickell GCMG, KCVO Chairman To be appointed Managing Editor and Deputy Chairman Dr David Frape BSc, PhD, PG Dip Agric, CBiol, FSB, FRCPath, RNutr. Mammalian physiologist Regional Editors in Chief Robert Cook BSc, CBiol, FSB. (UK) Plant pathologist and agronomist Professor Zhu Ming BS, PhD (China) President of CSAE & Seed and food drying and storage engineer 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 Xiuju Wei 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 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 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, FSB, 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, FSB, 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, FSB (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 Advisors to the board Dr John Bingham CBE, FRS, FRASE, ScD (UK) Crop geneticist

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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) Horiculuturalist Dr Philip Taylor BSc, MSc, PhD (UK)

WORLD AGRICULTURE

contents In this issue ... Dr Roger Turner obituary

Robert Cook

editorials: In This Issue – achieving a Low Carbon Economy

5-6

Dr David Frape

Conflicting Perspectives On GM – Science And Persuasion

What do we mean by Sustainable?

Policy And New Technology – Common Policy Problems

Professor Sir John Marsh Robert Cook

Professor Sir John Marsh

scientific: Contribution of improved nitrogen fertilizer use to development of a low carbon economy in China

10-18

Professor David Powlson, Professor David Norse, Professor David Chadwick, Dr Yuelai Lu, Dr Weifeng Zhang, Professor Fusuo Zhang, Professor Jikun Huang, Dr Xiangping Jia Agroecosystem management in arid areas under climate change: Experiences from the Semiarid Loess Plateau, China

19-29

Dr Rui-Ying Guo and Professor Feng-Min Li Interactions between orogeny, climate and land use in the Semiarid Loess Plateau, China

30-31

Dr Pete Falloon Plastic-film mulch in Chinese agriculture: Importance and problems

32-36

Professor Yan Changrong, Dr. He Wenqing, Professor Neil C. Turner, Dr. Liu Enke, Liu Qin, Liu Shuang

Aquaculture: are the criticisms justified? II – Aquaculture’s environmental impact and use of resources, with special reference to farming Atlantic salmon 37-52

Dr C J Shepherd and Professor D C Little

expected future contributions: Dr Penelope Bebeli – Landraces in Greece. Dr Michael Turner – Seed policies in guiding seed sector development in the ‘post project era’. Professor Wallace Cowling – Plant breeding systems for dry land Australia. 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 Cover photo – Overview of salmon farm, Isle of Skye – note feed barge to the right of the pens (Courtesy of Marine Harvest Ltd., Scotland)

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

the GM debate: Pros and cons of GM crops as a source of resistance to insect pests

53-59

GM is a valuable technology that solves many agricultural problems in breeding and generation of new traits

60-67

Professor Helmut van Emden

Professor Anthony Trewavas and Martin Livermore Response to Professor Anthony Trewavas & Martin Livermore

68-69

In defence of GM crops

70-71

Dr Helen Wallace

Professor Anthony Trewavas and Martin Livermore

economics and social: Mitigation of water logging and salinity through biodrainage: potential and practice

72-77

Professor O.P.Toky and Dr R. Angrish Scaling Up Technology Adoption Among Poor Farmers: the Case of Seed

78-83

Dr Sara Boettiger Problems of ‘Scaling up’ new crop cultivars: thoughts of an agricultural economist on wider issues in this interconnected world

Professor Sir John Marsh Smart Metrics and Data Management Strategies for Public Private Partnerships

85-86

Dr Sara Boettiger

WORLD AGRICULTURE 3

obituary

Dr Roger Turner Robert Cook

t is with great sadness that we report the death of Roger, one of our editors since the journal started. Roger made a great contribution to the technical revolution that swept through arable farming during the last decades of the 20th Century. As a researcher and a research manager he not only helped to develop the industry, but was a great exponent using technology to improve production efficiency and output. The early part of his career was spent with Shell Agriculture near Sittingbourne, Kent, where he joined the herbicide development team in 1967. He later worked in the Shell centre in London and then in the 1980s, was director of their field station in Cambridgeshire. After Shell closed their agricultural business he became Chief Executive of the British Association of Plant Breeders. He was responsible for a number of significant developments within the seed industry, not the least of which was the royalty scheme and arrangements for use of farm saved seed. As a scientist he was not only well liked and respected by his colleagues, but also made a significant contribution to the dissemination of

Dr Roger Turner

knowledge as an editor of several journals. He also served on the board of Rothamsted Research for a number of years. In addition to a successful career in

agriculture he was involved in his local community as a churchwarden in Mildenhall and was a devoted family man. We send or deepest sympathy to his widow, children and grandchildren.

Welcome to new Editorial Board members On behalf of my colleagues I should like to welcome fourteen new members to our Editorial Board (see page 2). These are all leaders in their fields of knowledge who, in alphabetical order, are from: Australia, Canada, China, India, Sri Lanka, United Arab Emirates, UK, and the USA. World Agriculture now has

4 WORLD AGRICULTURE

individuals on its Board with expert knowledge in various fields of botany, meteorology, engineering, nutrition, plant and animal physiology, veterinary medicine, both animal and human immunology, genetics, soil and plant & forest ecology, agroforestry & forestry, forensic chemistry, agricultural economics & sociology, teaching, and

biodiversity. This breadth of knowledge should allow us to deal effectively with many of the interactions and interrelationships agricultural production has with a changing climate and an increasing world population. David Frape

editorials

In This Issue – achieving a Low Carbon Economy David Frape

n this Issue we have international cooperation amongst nations of the kind this Journal was designed to kindle. Experts from China, UK, Australia and India have integrated and focused their attention on several current problems of international concern, the solutions to which will have widespread effects, not only for agricultural production, but also for issues of both economy and biodiversity. In this Issue we have conducted a detailed survey of many aspects of the semi-arid Loess Plateau in north-west China. In four papers the orogeny, climate, greenhouse gases, pollution, population & society and forestry of this area are discussed and ways forward are proposed. We continue our discussion of the vital subject of the nitrogen cycle. Previously in this Journal, Professor Vaclav Smil (1) concluded that approximately seven percent of manmade energy is employed in the fixation of atmospheric N2, as NH3,

by the Haber Bosch process and that approximately 40 percent of the human race depend on the N-fertilizer industry for adequate food to sustain their lives. Without that industry it would have not been possible for the human race to expand in the way it has during the 20th century. We all look forward to the time when atmospheric – N can be fixed industrially by a more direct use of solar energy, contributing immensely to a low carbon economy. Industrial fixation of N2 will have to increase, not only to accommodate an increasing human population, but to compensate for a possible decline in natural N-fixation as the poplulation of oceanic phytoplankton declines. N ferilizers are essential for the crop yields we now expect. Without N fertilizers it would be impossible to feed the current human and livestock populations of the world. Nevertheless, where the use of these ferilizers is subsidised there is the risk of their excessive use (see Powlson et al. this Issue, pages 10-18). This can lead to pollution of ground water, and the excessive production of nitrogen

Landscape of Shangri-La tibetan village

oxides which are the most potent of greenhouse gases, in addtion to the waste of fossil carbon energy in the production of NH3. Powlson et al. propose there is an urgent need for three sets of key changes in China if the management of N fertilisers is to increase significantly, improving economy and reducing both pollution and GHG emissions: 1. Radical changes in the way that information is communicated to farmers. 2. Changes in Government policies relating to subsidies for the manufacture and use of N fertiliser. 3. Measures to increase farm size and professionalism of farmers. Of these they consider points (2) and (3) to be much more important. The ecology and loss of the economic potential of the arid Loess plateau, of China, as a source of crops for food production and for plant growth generally, is of very great concern to the Government of China and to our scientists and economists generally.This subject is detailed in this Issue (pages 19-29). From the point of view of plant growth, the climate of this area has been deteriorating over centuries, owing

partly to the loss of forest trees. The causes of this deterioration are discussed by our meteorologist (pages 30-31). We also discuss the use in India of planted trees to help drainage of water-logged land, by acting as natural water pumps (see pages 72-77). A polythene mulch to retain moisture and heat in the soil to extend forward the growing season is a universal agricultural instrument for several crops. Whilst increasing yields this procedure has several drawbacks. These have been widely studied, especially in China, where a heavy gauge polythene is currently in use. Thicker material not only costs more, and is an oil-based product, but it persists longer in the soil pofile causing pollution and ultimately, following several years of continuous use, it may cause a depression in yield of crops. These effects have been measured by Chinese scientists and are discussed with solutions proposed in this Issue (see pp. 32-36 & 19-29). As a consequence of over-fishing, and with a decrease in O2 tension in the upper layers of the sea, and also as oceans gradually become more acidic, owing to an increase in the

WORLD AGRICULTURE 5

editorials partial pressure of atmospheric CO2, wild fish stocks and fish production will continue to decline. This emphasises the vital importance of fish farming – which will soon exceed oceanic fishing as a food source for the human race. Moreover, as fish are cold-blooded and are buoyed up by water they have considerably lower maintenance energy needs than do land animals. We discuss this subject in detail (see pp. 37-52 for the second paper in the series). We are again devoting space to the GM crop debate and include a fascinating paper (van Emden, pp.5359) on the control of insect pests by GM and pesticide means. It is vital that world-wide decision and policy makers understand the arguments both for and against GM. In my view it is quite irrational, to condem a whole field of science for

Landscape of Shangri-La tibetan village

6 WORLD AGRICULTURE

reasons of heresay statements and prejudice, rather than to base judgements on substansive peerreviewed evidence and rational discussion. There can be arguments both for and against individual procedures, but not for an entire field of knowledge. Hence, it is our opinion that these issues should be aired and that sound, rational conclusions should be reached- a major function of this Journal. New cultivars of crops, whether of GM or traditional origin, must be purchased by the farmer for sowing. Problems and procedures in the supply chain and scaling up of supply from the breeding firm to the farmer are also analysed in this Issue (pp. 78-83). Finally, research is becoming more and more expensive, so that the need for cooperation between groups is ever

more pressing. The procedures and problems encountered in Public-Private Partnerships of research work are discussed here (pp.85-86). In this Issue we are commenting to a much greater extent, than previously, on our papers to initiate discussion on both suggested consequences of conclusions drawn and on the wider implications of these conclusions. Hence, we welcome sensible comment from readers, either as Letters to the Editor, or more formally in our peerreviewed, Comment & Opinion Section. Please, let us know your views. These should be addressed to the editor: editor@world-agriculture.net

Reference 1. Smil, V. World Agriculture (2011) Nitrogen cycle and world food production, Vol. 2, No.1, pp 9-13.

editorials

Conflicting Perspectives On GM – Science And Persuasion Professor Sir John Marsh © DrUGO_1.0 – Fotolia.com

n January 17th 2014 a demonstration took place outside the Greenpeace offices in Hamburg. It was led by a group of scientists who were protesting against Greenpeace’s opposition to Golden Rice. This is genetically modified rice that provides a rich source of Vitamin A (as ß-carotene), essential for human health but not sufficiently available in the diets of many poor people whose staple food is rice. Greenpeace’s resistance to genetically modified food has taken the form of political action which has resulted in legislation to restrict use of GM crops and their produce in Europe . Their action is also associated with demonstrations against field trials of some modified crops, some leading to the destruction of experimental plots. It seems that the future for genetically modified food has become a contest to manipulate public opinion. Within the debate both sides claim that ‘science’ supports their position. World Agriculture has welcomed authoritative papers from a leading opponent of GM technology, Dr Helen Wallace and from scientists who advocate its acceptance and practical use. In this issue we include a critical analysis of Dr Wallace’s paper by Professor Anthony Trewavas and Martin Livermore BA (Oxon), Director, The Scientific Alliance and Dr Wallace’s response. The issues involved are of global importance, especially for poor people. Growing population, the probability that global warming will diminish the productivity of some major food producing areas and the pressure to grow crops for fuel will limit food supplies. Rising real incomes among some populous countries where diets are being upgraded suggest that real food prices will rise. For those whose incomes do not keep pace there is a prospect of growing hardship and for those who lack resources either to grow or buy food, an increased risk of starvation. The world needs every means at its

disposal to produce a sustainable and sufficient increase in food output. Those who support GM technology believe that its use can make an important contribution to relieving this pressure. Several claims are involved. It will be possible to produce GM crops that can cope with less favourable growing conditions, including higher temperatures, less water and shorter growing seasons. Using the technology plants can resist common pests and diseases without the use of chemicals that can pollute the environment and are, in their production and application, energy intensive. The implication is that more food output would be possible using fewer resources than current production systems. The modification of plants may also improve their nutritional quality, for example in golden rice. Thus, the use of genetic modification is expected to make a direct contribution to improving human health and wealth. As with any new technology it is impossible to know fully the possible effects it may have, especially in the longer term. In this area, as in all others, our knowledge is provisional and will be enlarged by later research and analysis. Given so potent a new technology it is natural that many

wish to proceed slowly rather than unleash forces that later prove to be damaging and uncontrollable. We have therefore to take seriously those anxieties that do surface, whether these arise from scientific critiques, from social concerns or because new technologies infringe ideological convictions. In each of these areas of concern serious analysts can honestly come to differing conclusions. In such a situation it is vital that each explores the position of others in order to discover where the real disagreement originates and thereby to understand more fully the issues at stake. World Agriculture & Environment seeks to encourage such a discourse. We are grateful to the contributors to this edition for setting out their positions with clarity. It moves the debate from the barricades to a more rational and more productive form of discourse. We would welcome further contributions that take the discussion further. Such a conversation is helpful to those who are not themselves expert in genetic modification or involved in its commercial exploitation but have to take decisions which will determine our capacity to cope with the looming problem of global food shortage.

WORLD AGRICULTURE 7

editorials

What do we mean by Sustainable? Robert Cook Should we not in editorials pose areas in which solutions might lie and indicate the problems associated with their implementation?

n the last issue we published some estimates of how the world might be able to avoid mass starvation without reducing biodiversity (destroying the environment,), by use of balanced and constructed vegetarian diets. That article demonstrated that the world could feed itself in 2050, assuming the population changes envisaged by the UN. It also demonstrated that it is possible to develop more sustainable food systems, although the diets would inevitably be rather bland and uninteresting to the consumer. But it would mean a greater extent of food redistribution from temperate to tropical regions? The article demonstrated that large amounts of external energy would still be needed to produce the fertilizers needed for crop production. It made no estimates of the energy needed for other tasks such as cultivations or crop protection, whether provided by man or machine, or of needs for transport, refrigeration or marketing. In order to develop a fully sustainable system, these energy needs should be met from replaceable systems. However, things are not as simple as this. If we assume economies continue to grow demand for more and different foods will increase. That will put further pressure of food production. One of these changes which might be anticipated is that people will wish to eat more meat. That will also increase demand on the food production system, simply because the energy and water requirements of livestock production are so great. Modern life is complex and sophisticated. The infrastructure of the food chain enables Western consumers to have a wide choice of produce throughout the year. However, in large parts of the world humans are already in food deficit, simply because of production constraints, irrespective of conflict. It suggests that already one might be able to argue that any system which limits the output per unit area might be unethical or immoral. We have constructed a communication system which provides instant, detailed information about

8 WORLD AGRICULTURE

diverse issues. Presentations in the media often seek to contrast the differences which emerge in complex debates, rather than inform of the complexities or attempt to find common ground. Climate change provides an excellent example. This is a complex subject. Subtle changes to the earth’s atmosphere and orbit, as well as solar activity, have significant impacts, the full effects of which may take hundreds of years to develop, so climates change over time. The consensus of informed scientific opinion recognizes that subtle changes to the atmosphere, made by man over many centuries, also affect the earth’s heat balance, leading to general recognition of anthropogenic impacts. How we respond to these changes attracts significant debate, not just because there are economic implications, but also because any adaptations to our life style or activity needs to be universally acceptable to have any chance of reducing the effects of so called global warming. This is the big problem – “I’m alright Jack”. There is no universal overlord instructing countries what they must do to offset potential problems for which the level of risk of their occurrence is uncertain, until it will be too late to take effective action – that action could mean a lower standard of living at present in order to prevent a possible catastrophic effect on living

standards for some future generations – it is nigh impossible for any single democratic government to institute a state of affairs that would be political suicide and put a country at an economic disadvantage vis à vis other competing countries, e.g. green energy policy.) Debates about feeding the world are similarly complex. Factors such as land availability, changing climates, human nutrition and agricultural technology have fundamental impacts individually and when considered in concert. The problem associated with these factors shares with climate change the fact that each of the factors interacts with one another so it becomes difficult to communicate not just the complexity of the problem but also the multiple levels of interactions*. This makes it difficult for the informed specialist to present the facts in simple, readily understood ways, not only to policy makers but also to the general public, who need facts to help them understand ‘the big picture’. *Examples are: “are the current floods/storms in the UK caused by climate change?” “Is climate change man made”. Therefore if we stop using fossil fuels will these storms be a thing of the past – Yes of course they will never occur again ah? This journal highlights these issues and helps readers to comprehend the complex factors and we hope

Editorials

Policy And New Technology â&#x20AC;&#x201C; Common Policy Problems Professor Sir John Marsh

his edition of WA includes a paper by Powlson and colleagues that looks in depth at the use of Nitrogenous fertiliser in China. Its conclusions are of immediate relevance to improving both the efficiency of Chinese agriculture and its impact on the environment. The paper also illustrates some general problems that apply to agricultural policy in China and in Europe. Subsidies and the creation of a dependent clientele. Fertiliser subsidies seem a good way to encourage its use, especially where for farmers it is a new technology. However they can lead to a situation where agriculture comes to depend on continued support, even if fertiliser applications are excessive. Not only farmers but also fertiliser manufacturers, distributors and advisors become clients of the support system. A reduction or withdrawal of subsidies then generates social and political problems. Jobs may be lost and incomes fall, since markets will not reward current rates of us. Employment in most agricultural communities is dispersed making it difficult, especially in remote areas, to find alternative work within reach of the homes of displaced farmers and farm workers. Support initially given to encourage output, as with the CAP, becomes difficult to remove because of its social and political consequences. New technologies demand structural adjustment. Innovative technology lowers costs of production for an industry but businesses that cannot use it efficiently become uncompetitive. Traditional farming is labour intensive and in most places a family enterprise. New technology usually replaces labour by capital. It also increases the scale and geographic range of markets. Small, independent, scattered holdings cannot reduce labour costs or deliver the volume of product large marketing organisations seek to buy. This study shows how in China the use of contractors to deliver and apply

fertiliser has been used to counteract some of the limitations of small-scale farming. However, viability of such farm businesses depends on employment off the farm. Where this is not possible technological development needed to make a nationâ&#x20AC;&#x2122;s agriculture more productive may impoverish remote, small farms. Where farming becomes only a subsidiary source of income husbandry standards are unlikely to be maintained. Structural adjustment through farm enlargement depends greatly on the ownership of the land and prevailing systems of tenancy. For family farms it is often a painful process. At a national level it lags behind the pattern needed to obtain maximum economic benefit from current technology Policies relating to technological development have to be assessed in terms of social costs and benefits. Innovation will be profitable for the farmer if additional costs are less than returns. Such calculations determine the decision to invest, but usually ignore costs or benefits that do not figure in the farmâ&#x20AC;&#x2122;s financial accounts. Farmers, themselves, are often influenced by such non-market costs. They may want to find work for a family member. They may value a particular landscape feature or simply enjoy being farmers. For society as a whole such non-market costs and benefits have been increasingly recognised. Environmentalists have deplored the impact of some modern farming practices on biodiversity, wildlife, water quality and the landscape. Pressure groups have made it clear that these are real costs although they do not figure in management accounts. There are other types of social costs. The costs per unit of providing services such as education and health rise, as people have to move to find employment. The informal support given to the elderly within traditional communities may disappear as families are separated. Conceptually the principal justification for policy intervention is to make social costs and returns

influence the decisions of farmers and consumers. In practice this is difficult. Recognition of non-market costs and returns often depends on the existence of articulate pressure groups rather than on the impact of policies on the whole community. Powerful and well-informed pressure groups command a hearing when national policies are debated. Organisations such as RSPB*, RSPCA** and CPRE*** have widespread support and claim attention for the interests they represent. Local activists may be regarded as NIMBYs, and carry little weight on national policies. Some social costs and benefits such as the loss of village schools and shops, or the state of rural roads attract much less organised campaigns. Even when costs and benefits are identified there is seldom an objective or agreed means to measure them. The outcome is that policy tends to reflect the concerns of organisations that can claim to speak for a large number of members. Such membership is largely urban or sub-urban. There is less interest in farming as a business and more on the countryside as an amenity. Traditional literature and visual attractiveness in television programs take precedence over present farm business reality. Such concerns have stimulated policies to prevent hunting with dogs, to give ramblers rights of access and to impose restrictions on the use of GM technology. It is argued that such policies are justified because the non-market benefit to the community is larger than the costs, financial and non-market, they impose on the industry. The debate on such issues, and in general the uptake of new technology, may depend less on scientific analysis or economic benefit than on the political clout of interested parties. * Royal Society for the Protection of Birds ** Royal Society for the Prevention of Cruelty to Animals *** Campaign to Protect Rural England.

WORLD AGRICULTURE 9

scientific

Contribution of improved nitrogen fertilizer use to development of a low carbon economy in China Professor David Powlson1, Professor David Norse2, Professor David Chadwick3, Dr Yuelai Lu4, Dr Weifeng Zhang5, Professor Fusuo Zhang5, Professor Jikun Huang6, Dr Xiangping Jia6 1 Rothamsted Research, UK. 2 UCL Environment Institute, University College, London, UK. 3 Bangor University, UK. 4 University of East Anglia, UK. 5 China Agricultural University, China. 6 Centre for Chinese Agricultural Policy, Chinese Academy of Sciences, China. Summary The use of nitrogen (N) and other fertilisers has been one of the keys to achieving food security in China. Grain production almost doubled in China between 1980 and 2010, yet total fertiliser use increased more than four-fold in the same period. This disparity is partly due to changes in cropping, with a large increase in the area devoted to horticultural crops (vegetables and fruit trees) that are given large rates of fertiliser, especially N. But it also reflects the extremely high rates of N application given to a wide range of crops, including cereals. There is overwhelming evidence that rates of N applied to many crops in many regions of China are greatly in excess of the rates required to achieve maximum economic yield. These excessively high rates, combined with inappropriate fertiliser management practices such as timing and method of application, have led to very inefficient use of N and considerable losses to water and air with numerous adverse environmental impacts. A key reason for much of the inappropriate fertiliser management is that many farmers are parttime, with more lucrative income from off-farm work. Thus farm operations are given a low priority, with little incentive to change practices if these involve additional costs, or labour, that interferes with the off-farm work. In this article we review the current situation regarding N fertiliser in China, with an emphasis on the reductions in greenhouse gas emissions that are achievable through changes in both manufacturing and agricultural use. We argue that, although technical innovations have a role, these are only likely to be widely adopted in practice if policy changes are implemented to promote changes in fertiliser manufacturing and on the farm. Necessary changes in policy include changes to the subsidy, originally developed to make fertilisers affordable to farmers in the period before rapid economic development in the country. At the farm level, policies to promote greater professionalism in farming through increasing the size of farms will facilitate more rational use of N. This is possible as large numbers of former farmers move to other work in cities; the Chinese government has policy initiatives in this area through changes in land rental arrangements. Another welcome change would be measures to promote more farmer-oriented approaches to the delivery of technical advice such as the farmer field-school approach, and development of a contractor sector for fertiliser application. Key words China, fertilisers, nitrogen, pollution, nitrate, nitrous oxide, greenhouse gas emissions

Abbreviations

GHG greenhouse gas; IPCC Intergovernmental Panel on Climate Change; Mt million tonnes; Tg tera grammes, equal to

1012g or 1 Mt

Glossary Emission factor (EF): is a measure of the average emission rate of a given greenhouse gas (GHG) from a given source material in a given context. In this article it is used to describe the

Introduction

hina has been extremely successful in achieving food security through a set of government-initiated measures introduced over several decades. For many years there was a de facto

10 WORLD AGRICULTURE

proportion of the nitrogen (N) from sources including fertiliser, manure or biologically fixed N that is converted to nitrous oxide (N2O) when applied to soil. EFs are always expressed as proportion of the source substance converted to the GHG in question, so if

1% of applied fertiliser N is converted to N2O the EF is 0.01. Eutrophication: a dense growth of aquatic plant life caused by excessive richness of nutrients in a lake or other body of water, frequently due to runoff from the land.

policy of aiming at close to 100% selfsufficiency in basic food crops: in 1996 the policy was modified and a target of at least 95% self-sufficiency in grains was formally adopted. The measures adopted during the last 30-40 years to achieve food security have included provision of new crop

cultivars to farmers, installation of infrastructure such as irrigation schemes, subsidies to fertiliser manufacturers to limit the price of fertilisers to farmers, and various subsidies to farmers to enable them to purchase inputs such as fertilisers, pesticides and machinery.

scientific The use of fertilisers, especially nitrogen (N), has been a major factor in achieving food security – so the policies to make it available and affordable have been successful. But there is now overwhelming evidence of N fertiliser being applied at excessive rates and in ways that lead to its inefficient use and large losses to the environment, with a wide range of damaging environmental and economic impacts. These excessive rates are a major cause of agriculture overtaking industry as the main source of pollution (1), and this is estimated to be causing a reduction in national GDP of about 1%. The situation could be termed an “overshoot”; policies that were entirely appropriate in the past have served their purpose, successfully, but are no longer helpful and are having unintended and perverse consequences. This paper briefly reviews the evidence for current over-use and misuse of N fertiliser in China and the environmental and economic benefits to be gained from a move to a more rational use. We emphasise the reductions in greenhouse gas (GHG) emissions to be derived from reduced use because this aspect has previously received less attention than has water pollution. We conclude that changes in policy are urgently required if a more rational use of N fertiliser is to be achieved – improved training of farmers is necessary, but is generally insufficient to alter behaviour, especially if not accompanied by appropriate policies and economic measures. A particular requirement is for a change in the current subsidy regime affecting N fertiliser. There are

Table 1. Fertiliser used (total of N+P+K) on different crops in China: changes between 1998 and 2008. Values shown are quantity of fertiliser applied to each group of crops and this quantity expressed as a percentage of the total used on all crops.

strong moves in China to develop a greener economy, with lower GHG emissions per unit of production, or of economic output, but the large and very cost-effective contribution that is possible from agriculture is often not recognised.

Nitrogen fertiliser use – present situation Figure 1 shows the increase in total production of grain (wheat, maize, rice) and the use of fertilisers (total of N, P and K) between 1980 and 2010. Grain production increased to 170% of its 1980 level but the corresponding increase in fertilizer use was 438%. In part this is a reflection of increasingly inefficient use of fertilisers but it also results from a major change in cropping patterns over the period. There has been a large increase in production of horticultural crops (vegetables and fruit), both in open fields and under plastic. Table 1 shows changes in the amounts of fertiliser (total of N, P and K) applied to different classes of crop

Figure 1. Changes in total fertiliser use (total of N+P+K) (grey) and grain production (total of wheat, maize and rice) (yellow) in China between 1980 and 2010. Values in 1980 set at 100.

over the ten year period, 1998 to 2008. The amount applied to vegetables almost trebled and that to fruit crops doubled; this partly reflects the greatly increased area of these crops and partly the very large rates of fertiliser (especially N) applied to them. There is a particular issue with N fertiliser being applied at rates in excess of that required to achieve maximum yield. There are numerous examples of this for all major crops in most regions of China. Overapplication, and a range of inappropriate management practices, have led to very inefficient use of N fertilizer by crops in China. Figure 2 shows the partial factor productivity for N (PFPN) of grain crops in China over the period 1980 to 2005. PFPN is the ratio of grain produced to N applied so a larger number represents a more efficient use of N fertiliser. During the 25 year period shown, the value of PFPN decreased by half from 34 kg grain kg1 N applied when N rates were low in the early 1980s to about 15 kg grain kg-1 N in recent years. For comparison, the PFPN for maize in the USA increased from about 40 to almost 60 kg grain kg-1 N between 1980 and 2000 (2). Fortunately, there is widespread evidence that reduced application of N fertilizer, often combined with changes in timing or other management factors, can achieve the same crop yields as current excessive applications. In one study, two major cropping systems of great importance to China’s food security were investigated: the rice-wheat system as practiced in the Yangtze River basin in Jiangsu Province and the maize-wheat rotation in the North China Plain. (3). The authors concluded that current crop yields could be maintained with reductions of 30-60% in N fertilizer applications.

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Figure 2. Changes in annual N fertiliser consumption, grain production and partial factor productivity of N (PFPN) in China between 1980 and 2008. PFPN is the ratio of grain produced to fertiliser N consumed expressed as kg grain kg-1 N.

Another study on rice in 20 farms in the Yangtze basin, this time in Zhejiang Province, showed that in one year N applications to rice could be reduced from 300 to 150 kg N ha-1 with no loss of yield (4). In other years and sites reductions of about 30% were more common. In the North China Plain a study on N fertilisation of winter wheat (5) showed that by basing N applications on measurements of mineral N in soil total applications could be reduced to 55-65 kg N ha-1, with no loss of yield, instead of the farmers’ practice of 300 kg N ha-1. This dramatic result was because of large residues of nitrate in the soil, unused from previous years which are normally ignored, or are lost due to excessive irrigation. Such large savings are unlikely to be sustained indefinitely, but reductions of 30-50% compared to current common practice, as shown in other studies, are considered

sustainable in the long term. Management practices such as timing are also important for increasing the efficiency of use of applied N; in the study previously cited (5) it was found that, with current rates of N, crop yields could be doubled compared with farmers’ yields through a set of management changes. Single year experiments demonstrating that yields are maintained with reduced N application can, correctly, be criticised as being a reflection of nitrate accumulated in the soil over many years and thus not repeatable in future years. However, long-term experiments clearly show that high yields can be sustained with N rates that are significantly lower than current common practice. For example, at one site in Henan Province, in the North China Plain (part of an 8-site national network of experiments), yields of wheat in the

Table 2. Examples of N fertiliser over-use for various crops in different regions of China (from (7)).

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wheat-maize double crop rotation were sustained at 6-8 t ha-1for 15 years with an annual N application of 165 kg N ha-1. This rate is far lower than commonly observed in the region, that are well in excess of 200 kg N ha (6). Table 2 (from Norse et al., (7)) summarises results for a range of crops in various regions of China which demonstrate that substantial savings of N fertiliser can be made. Not only is crop yield not decreased, there is often a modest yield increase. A small increase in yield compared to crops receiving excessive N fertilizer is not unexpected because it well known that crops over-supplied with N are more susceptible to pests and diseases (8), so a more rational N management should lead to decreased use of pesticides with wider benefits for the environment and human health, in addition tofinancial gain for the farmer. Crops over-supplied with N can also be more prone to “lodging” where crops fall over, due to weakness of the stems, making harvesting more difficult, and so leading to loss of grain. In addition, research at China Agricultural University has shown than maize plants receiving a super-optimal amount of N fertiliser have a smaller root system than that of correctly fertilised plants (Figure 3). Over-use of N fertiliser in China has serious impacts on land, water and air at the local, regional and global level.

Figure 3. Effect of N fertiliser overapplication on growth of maize roots. (a) Roots of over-fertilised plants. (b) Roots of plants given a rational rate of N fertiliser. (Photo by C.J. Li, China Agricultural University, Beijing).

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Figure 4. Lake eutophication and algal growth caused by run-off of nitrate and phosphate from agricultural land.

Soil acidification has doubled over the past 30 years, to which N fertilizer has contributed about 60% (9). Much of the acidification stems from the high inputs of ammonium-based N fertilizer such as urea and the uptake and removal of base cations rather than from acid rain. However, in view of the rapid increase in animal numbers in recent years, ammonia emissions from manure and other livestock wastes may become of increasing importance. The crop yield and food security impacts of acidification include suppression of rhizobial activity and reduced availability of micro-nutrients, in addition to direct impacts of acidification on crop growth. The outcome is a threat to the sustainability of Chinese agriculture. In the case of surface waters, nitrate entering rivers and lakes (together with phosphate, often derived from poor management of manure) leads to algal blooms, the growth of water weeds and widespread eutrophication. More than 50% of China’s major lakes are now eutrophic and for most of them the situation is getting worse (10). The incidence of algal blooms has increased several-fold since the 1990s and agriculture is responsible for 2580% of N inputs to major rivers which, in turn, are damaging to fisheries and so damage food security in a different sector. With both surface waters and ground waters, nitrate not taken up by crops leads to high concentrations in water used for drinking, which often exceed WHO guidelines for drinking water. Algal blooms themselves also pose a health threat to animals and humans due to production of potent

Figure 5. Results from a survey of “sunlight greenhouses” in a region near Xi’an city in northwest China. These are greenhouses used for growing a range of high-value horticultural crops under plastic, often two or three crops each year. The plastic is removed during the summer rainy period to expose the soil to rainfall so that accumulated salts are washed out. Results are mainly from greenhouses growing tomatoes, 116 being surveyed to determine rates of N fertiliser applied by the farmer and 43 being measured for nitrate accumulated in soil. Data plotted show the frequency distribution of (a) N fertiliser application rates and (b) residual nitrate (kg nitrate-N ha-1) in soil to a depth of 1m. Both are expressed as a percentage of the total number of greenhouses surveyed (From 16).

toxins by the cyanobacteria (also known as blue-green algae) that comprise the blooms. The impact can be direct through drinking of the water (11, 12) or through the food chain, especially via shellfish (13) and the occurrence of cyanobacterial blooms is likely to increase under the influence of climate change (14). Finally there is the important impact on air quality, particularly the emissions of ammonia that lead to particulate formation with resulting implications for human health (15), eutrophication of natural and semi-natural aquatic and terrestrial systems, soil acidification as described above and to the greenhouse gas emissions examined in the next section. Figure 5a illustrates the situation

regarding high rates of N fertiliser applied to horticultural crops. The data are from a survey of farmers growing tomatoes under plastic in so-called “sunlight greenhouses” of the suburbs of Xi’an city in northwest China (16). The greenhouse structure is covered with plastic for part of the year to provide a protected environment and increased temperature for growing a range of horticultural crops including tomatoes, cucumbers, courgettes (zucchini), aubergines (egg plant) and peppers that have a high value. The plastic is removed from the structures during summer, when rainfall is relatively high and the higher temperature is not needed. Salts accumulated in the soil are leached out of the topsoil during this period.

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scientific Of the 116 greenhouses surveyed in an area near Xi’an city, 65% of farmers were applying in excess of 400 kg N ha-1 with a quarter applying >800 kg N ha-1. These rates are extremely high by international standards and were in addition to large annual manure applications estimated to be supplying almost 1000 kg N ha-1. Not surprisingly these management practices led to very large residues of nitrate in soil. More than 60% of sites where soil was analysed contained >350 kg N ha-1 as nitrate-N in the soil to a depth of 1m (Figure 5b). The issue of inefficient use of nutrients from manure has recently been reviewed and proposals made for addressing the problem (17), as manure applications are generally ignored when farmers make decisions on application rates of fertilizer.

Greenhouse gas emission associated with nitrogen fertiliser Nitrogen fertiliser inevitably has a large greenhouse gas footprint with emissions from the following sources: 1. Carbon dioxide (CO2) emitted during manufacture, especially from the ammonia production stage using the Haber-Bosch process because this requires a large amount of energy to achieve the necessary high temperature and pressure. The energy is provided largely by fossil fuels, usually natural gas or coal. In China coal is the dominant energy source. 2. Emissions of nitrous oxide (N2O) when N fertiliser is applied to soil. Typically the quantity evolved is small, 1% or less of the N applied, but N2O is a very powerful greenhouse gas; each molecule is almost 300 times more powerful in global warming than a molecule of CO2, so even small emissions have large impacts. Emissions of N2O from the field where N is applied are termed “direct emissions”. Emission can vary widely according to climate, soil type and environmental factors. The gas can be produced from two separate processes in soil, nitrification and denitrification. Nitrification is the conversion of ammonium to nitrate and is a dominant process in most soils except those that are water-logged (as in flooded rice cultivation), or in soils that are very acid. Denitrification is the reduction of nitrate to a mixture of N2O and nitrogen gas, normally in soils under wet conditions in which oxygen is limiting. It is often the main source of N2O from soils, but in the

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Table 3. Greenhouse gas (GHG) emissions associated with the N fertiliser chain in China including manufacture, transportation and agricultural use of N fertiliser (adapted from (26)).

dry conditions of north China there is evidence that nitrification is the major pathway (18, 19). 3. “Indirect emissions” of N2O. These arise from transformations of N that has moved from the site of fertiliser application. For example, nitrate leached from surface soil to deeper layers or to waterways can be denitrified later. Ammonia volatilised from the soil surface after applying urea is redeposited onto soil and water elsewhere and undergoes nitrification and denitrification. The IPCC derived an average value of 1% of N applied for the direct emission of N2O at the site of fertiliser or manure application, based on a review of world literature (20). This is termed the “emission factor”, EF. Later reviews (21, 22) have suggested an EF value that takes into account total N2O emissions (direct + indirect) in the range 2-5% of applied N. Widely accepted values for the total greenhouse gas impact of N fertilisers, combining emissions from both manufacture (under European conditions) and agricultural use are 10.5 kg CO2-equivalent per kg N in urea and a corresponding figure of 8.4 for ammonium nitrate (23). A clear implication of this large value is that it is essential to use N fertiliser efficiently, so that emissions are no larger than absolutely necessary. Some might argue that a strategy of eliminating all use of N fertiliser would be an effective way of decreasing emissions from agriculture, but this would have a devastating impact on global food security. One estimate (24) is that agricultural systems using no chemical fertilisers could, on optimistic

assumptions, feed only 4.2 billion people or 60% of the current world population and less than 50% of the population expected by 2050. The concept of “yield-scaled N2O emissions” has been introduced as a way of expressing the N2O efficiency of a cropping system (25). A global meta-analysis of nonleguminous annual crops showed that N2O emissions expressed as a proportion of crop N uptake (this being used as a proxy for yields across the diverse crops included) were at a minimum at N fertiliser application rates of approximately 180–190 kg N ha-1 and emissions increased sharply after that – for example 3-fold greater for applications rates > 300 kg N ha-1 (25). N applications that are very low or near zero give increased values for yield-scaled N2O emission because yield is low. The N application rate giving a minimum value of yield-scaled N2O emission was often about the same rate as recommended for maximum economic yield and there was a negative relationship between N use efficiency and yield-scaled N2O emissions. These findings further emphasise the importance of aiming at rational N fertiliser rates as a means of decreasing GHG emissions – but they do not lend support to the idea of eliminating N fertiliser. And even where fertiliser can be replaced by manures or biologically fixed N, N2O emissions still occur (22. 21, 22). In a recent study by Zhang et al. (26) a life cycle approach was taken to quantify the GHG emissions associated with N fertiliser in China; the results are summarised in Table 3.

scientific The total GHG emission associated with N fertiliser (both manufacture and use) was estimated at 452 Mt CO2equivalent in 2010, representing 7% of emissions from the entire Chinese economy (26). Emissions per kg of N fertiliser manufactured and used in China (13.5 kg CO2-equivalent kg-1 N) are higher than corresponding values from elsewhere in the world such as Europe (10.5 kg CO2-equivalent kg-1 for ureaN) for two main reasons. First, coal is the dominant source of energy used in N fertiliser manufacture in China, accounting for 86% of energy use (26). CO2 emissions per unit of energy are greater for coal than for natural gas which is the main source of energy for fertiliser manufacture in Europe and most other regions. In addition to CO2 emitted from the fertiliser plant, the life cycle approach means that the significant methane emissions from the mining of coal should also be included in the accounting. Second, 64% of fertiliser manufacture in China occurs in small plants using old technology (26); for any energy source (coal, oil or natural gas) these plants are less efficient and give larger emissions per unit of N fertiliser produced than larger plants utilising modern technology.

Options for decreasing GHG emissions connected with N fertilisers in China Fertiliser manufacture

When seeking to identify opportunities for decreasing GHG emissions from agriculture, especially those associated with N fertiliser, it is common to focus solely on management practices at farm level. Whilst these are extremely important, the results in Table 3 show clearly that it is also appropriate to consider emissions at the manufacturing stage; in China these account for over 60% of the total emissions from the N fertiliser chain (or 38% if methane from coal mining is excluded). A complete switch from coal to natural gas is not a practical option because China has large reserves of coal but a shortage of domestically sourced natural gas. Consequently changes in the fertiliser manufacturing sector will have to focus on the following: 1. Phasing out small factories which may often cause local air pollution with negative impacts on human health as well as being large GHG emitters. 2. Upgrading technology in existing larger factories. 3. Consider installation of “carbon

capture and storage” (CCS) at the largest coal fired factories. All of these measures will require government action in the form of changes to subsidies (27), including removal of support for small scale plants and incentives to upgrade others, but the potential impact is considerable. A set of scenarios were constructed in the study of Zhang et al. (27) to explore the decreases possible by 2020 and 2030 compared to “business as usual” (scenario 1) in which it was assumed that N fertiliser use would continue to increase in line with projected population increase. This showed that even without improvements in N use at farm level, improvements in the efficiency of the N fertiliser manufacturing process alone (scenario 2), could decrease GHG emissions by 20-30% compared to “business as usual” (Figure 6; these values did not assume major infrastructure installations such as CCS). Even if only a fraction of these GHG savings can be achieved, due to practical constraints, the analysis demonstrates that considerable savings, which are often overlooked, are potentially possible from fertiliser manufacture in China. Additional issues regarding the present subsidy regime are discussed later. Technical approaches to improve fertiliser management at farm level

Research in China has identified a range of management practices at farm level that would increase the efficiency of use of N fertiliser and/or

decrease N losses to the environment (27). These include the following: Adjust N application rate to a realistic assessment of crop needs, based on previous yields and taking account of the likely supply of N from soil. The latter includes N mineralised during the cropping season, residual nitrate in the soil profile andN from previous manure applications. As discussed above, there is a vast body of data showing that very significant savings of N can be made with no loss of crop yield – and in some cases small yield increases. Adopt sub-surface application of N fertiliser because surface application of urea, which is currently normal practice, frequently leads to large N losses to the atmosphere as ammonia. In one experiment conducted by China Agricultural University, this application method decreased ammonia losses at the time of urea application from 27% to 8%. In many situations it may be possible to alter the timing of N fertiliser application such that a greater proportion is given during the main growth period instead of at sowing, or transplanting in the case of transplanted paddy rice. Where farmers consider it impractical to adjust the timing of N application (often due to labour constraints at mid-season because of off-farm work use of either slow release forms of N fertiliser or forms containing inhibitors of either nitrification or urease activity in soil. (28, 29).

Figure 6. Greenhouse gas (GHG) emissions (expressed as CO2-equivalent) associated with the manufacture and use of N fertiliser in China. Emissions shown in units of Tg CO2-equivalent (1Tg = 1012g or 1 million tonnes). Emission estimates for 2020 and 2030 are for 4 scenarios. Scenario 1: “business as usual”; N fertiliser production and use increases in line with projected population increase, no changes in manufacturing processes or agricultural practices. Scenario 2: improved manufacturing technologies. Scenario 3: improved manufacturing technologies plus controlled N use on crops. Scenario 4: improved manufacturing technologies plus reduced N use on crops using all available methods (from 26).

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scientific In regions where soil and environmental conditions lead to significant emission of N2O through nitrification in soil use nitrate-based fertiliser instead of urea. Improve management of animal manures and other organic inputs such as residues from anaerobic digestion (the process used for producing biogas) at all stages in order to decrease N losses and maximise recovery of manure-derived N by crops (17). Taking account of manurederived N, decreasing fertiliser N application accordingly, is especially important where vegetable crops or fruit trees are grown, as these tend to receive large doses of manure. In regions where there is an excessive quantity of manure due to large animal numbers promote production of organic fertiliser products using aerobic composting and transport these to other regions as a partial substitute for inorganic fertilisers. Because of the cost of the composting process, this requires government subsidies to make it viable. Where irrigation is used, adopt “fertigation” in which nutrients are dissolved in irrigation water and delivered to crops during the growing period as this can greatly increase the efficiency of crop utilisation of nutrients. The practice is already used by some farmers growing horticultural crop under plastic but there is a need for greatly improved delivery of advice to ensure that the maximum benefit is obtained. There are also opportunities for extending the practice to irrigated crops grown in open fields, though additional engineering innovation would be required together with delivery of appropriate technical advice. Innovations necessary to facilitate changes in N fertiliser management

The benefit of many of the changes in N fertiliser management listed above has been known for many years and the changes have been proposed by researchers – yet very few have been adopted by farmers and, in the main, the situation of over-use, mis-use and inefficient use of N fertiliser in China has become progressively worse. Why? We suggest three sets of key changes that are required if the management of N fertiliser is to improve significantly: 1. Radical changes in the way that information is communicated to farmers. 2. Changes in Government policies relating to subsidies for the manufacture and use of N fertiliser.

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3. Measures to increase farm size and professionalism of farmers. We consider that the second two by far the more significant but we consider each in turn. Communication of fertiliser management information to farmers

It is often stated in China that the key to improving fertiliser management is to improve the delivery of technical advice to farmers. We consider this to be partially true, but certainly not the full answer. China has a large and established national extension system and in the past it has been effective in assisting farmers. But in recent years, for a range of organisational reasons, it has become ineffective: the reasons have been documented in detail elsewhere (30). It is now understood that extension messages delivered in the traditional mode of “expert tells farmer” are often ineffective. For example, a study based on household data collected from 813 maize farmers in Shandong Province showed that while training on rational fertiliser use (termed: integrated nutrient management, INM) could lead to some reduction in farmers' rates of N fertilizer application, training alone was not sufficient to change practices significantly and farmers only partially adopted the recommended INM (31, 32). An alternative model is the farmer field school in which “farmer tells farmer”, albeit facilitated by an “expert” or advisory agent. Evidence from around the world, as well as in China, demonstrates that this can be more effective. Although it has been applied in China with respect to pesticide use, as yet it has been little used for fertiliser management. Identifying early adopters and innovators would be key to adoption of these techniques. Changes in government policies regarding subsidies affecting fertiliser manufacture and use

Subsidies to keep down the cost of fertilisers were introduced to make these vital inputs affordable for small farmers. This policy has clearly succeeded and is no longer necessary. We propose that the general subsidy on fertilisers be removed and replaced by more targeted payments that are relevant to the current situation (10, 27). A major and positive innovation would be a scheme to promote the role of contractors in applying fertilizer. Virtually all the technical innovations discussed above have either an

economic cost (e.g. equipment for sub-surface application of urea), or require additional labour for applying N during the course of the growing season. Because so many farmers are engaged in off-farm work, that is usually far more lucrative than the income from farming a small area, they have no incentive to adopt practices that increase efficiency of N use. Reorganising subsidies such that a farmer had a payment for the use of a contractor, instead of for the cost of fertiliser, could make a major contribution to the improved management of N and other nutrients. It would be worthwhile for a contractor to purchase machinery for sub-surface fertilizer application whereas it is not so for an individual small farmer. And a contractor specialising in this work would be able to make timely applications, unhampered by labour shortages at key times, as often occurs for the parttime small farmers. There are already agricultural contractors operating in China, often using small combine harvesters and in some cases applying pesticides, so the extension to fertiliser application is not unreasonable – provided the policy and subsidy environment is arranged specifically to facilitate and promote the change. A similar approach could be extremely useful in promoting the efficient use of nutrients in manure, in terms of transportation and mechanised spreading (17). It would need to be cost-neutral for the farmer and ideally be attractive through a specific payment, at least initially. In practice contractors (termed “professional service providers” in China) are usually innovative farmers who decide to specialise in a specific type of work to increase their income. A further advantage of promoting this contractor sector is that it represents a cadre of more professionally skilled agricultural operators. They are more likely to be influenced by training programmes than the part-time farmers, who have off-farm priorities. Also, because their numbers would be smaller than the total of all farmers, the task of delivering relevant technical training is more tractable. However, there are challenges to this approach. For example, it is essential that a farmer has confidence in his or her contractor and trusts their judgment and honesty. Monitoring the performance of contractors is difficult under current conditions in China: development of

scientific certification or accreditation schemes will be an important development, possibly learning from the FACTS scheme for training and accreditation of fertilizer advisers in the UK which has backing from government agencies, fertiliser industry and farmers organisations (33). Measures to increase farm size and farmer professionalism

The importance of off-farm work for farmers presents challenges to good agricultural practice, as discussed above. But it also presents opportunities through the possibility of those wishing to concentrate on other work renting their land to neighbours who wish to specialise in farming. (In China it is a matter of land rental rather than sale because all land is owned the state). This trend leads to a gradual increase in farm size, termed “land consolidation”. It has been occurring for some years in China, initially through informal arrangements but later with official encouragement. There is evidence that farmers with a larger area use slightly lower rates of N fertiliser (31, 32), presumably because they are making farm management decisions in a more professional way. A recent Chinese government document on agricultural polices includes statements on measures “to speed up the transfer of rural land and offer more subsidies to family farms and farmer's cooperatives … in an effort to develop large-scale farming” (33). Policies of this type may well be the key to moving towards more rational use of N fertilisers and other desirable farm practices.

Conclusions Rapid changes in China, affecting both the general economy as well as practices within farming, have led to excessive N fertiliser use. The amounts applied to crops in many situations are now considerably greater than those required for maximum economic yield. The situation is particularly severe in the horticulture sector but even with the major cereal crops (wheat, maize, rice) it has been clearly demonstrated that reductions of 30% or more are often possible – with no loss in yield and often a small increase. In addition to excessive quantities being applied, management factors such as timing and method of application are often inappropriate and lead to inefficient use of N by crops, large losses to the environment and decreased profit to

farmers. There are numerous and well known technical approaches to improve the situation but these are unlikely to be adopted unless their promotion is accompanied by changes in policy and infrastructure to create a more professional approach to farming. These measures include changes to subsidy regimes, that were introduced to promote fertiliser use at a time when farmers could ill-afford such inputs, encouragement of a contractor sector for fertiliser management (to overcome labour shortages affecting many part-time farmers involved in more lucrative off-farm work) and measures leading to increased farm size through encouragement of the land rental market. Although improving delivery of advice to farmers, based on up-to-date scientific understanding, is important this will have limited impact if not accompanied by appropriate changes at the policy level. Improved management of N from fertilizers and manures is often seen as a means to improve water quality in China. The potential to cut greenhouse gas emissions and contribute to a low carbon economy, a goal of the Chinese government, is often overlooked. Recent research shows that cuts in emissions equivalent to between 2 and 6% of total emissions from the whole Chinese economy are possible through a combination of improvements in farm practice and N fertiliser manufacture.

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scientific 22. Davidson, E A (2009) The contribution of manure and fertilizer nitrogen to atmospheric nitrous oxide since 1860. Nature Geoscience 2: 659–62. 23. Brentrup, F, & Palliere, C (2008) GHG emission and energy efficiency in European nitrogen fertilizer production and use. Proceedings of the International Fertilizer Society, 639, 25 pp. 24. Connor, D J (2008) Organic agriculture cannot feed the world. Field Crops Research 106: 187–190. 25. van Groeningen, J W, Velthof, G L, Oenema, O, van Groeningen, K J, & van Kessel, C (2010) Towards an agronomic assessment of N2O emissions: a case study for arable crops. European Journal of Soil Science 61: 903-913. 26. Zhang, W-F, Dou, Z-X, He, P, Ju, X-T, Powlson, D S, Chadwick, D R, Norse, D, Lu, Y-L, Zhang, Y, Wu, L, Chen, X-P, Cassman, K G. & Zhang, F-S (2013). New technologies reduce greenhouse gas emissions from nitrogenous fertilizer in China. Proceedings of the National Academy of Sciences, USA 110: 8375-8380. 27. Powlson, D S, Zhang, F S, Zhang, W F, Huang, J, Norse, D, Chadwick, D R., & Lu, Y (2012) Policies and technologies to overcome excessive and inefficient use of nitrogen fertilizer: delivering

multiple benefits. Sain Policy Brief No. 5. http://www.sainonline.org/SAINWebsite(English)/download/PolicyBrief%20No%20 5%20Feb%202012.pdf 28. Kottagoda, N Munaweera, I, Madusanka, N, Sirisena, D, Amaratunga, G A J, & Karunaratne, V (2012) The advent of nanotechnology in smart fertiliser. World Agriculture, 3 (1): 27-31. 29. Watson, C J, Laughlin, R J, & McGeough, K L. (2009) Modification of nitrogen fertilisers using inhibitors: opportunities and potentials for improving nitrogen use efficiency. Proceedings of the International Fertiliser Society, 658, 40 pp. 30. Hu, R, Cai, Y, Chen, K Z., & Huang, J (2012) Effects of inclusive public agricultural extension service: Results from a policy reform experiment in western China. China Economic Review 23: 962974. 31. Jia, X P., Huang, J K., Xiang, C, Hou, L K, Zhang, F S, Chen, X P, Cai, Z L. & Bergmann, H (2013) Farmer's adoption of improved nitrogen management strategies in maize production in China: an experimental knowledge training. Journal of Integrative Agriculture 12: 364-333. 32. Huang, J, Xiang, C, Jia, X & Hu, R (2012) Impacts of training on farmers’ nitrogen use in

Longji rice terraces, Guangxi province, China

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maize production in Shandong, China. Journal of Soil and Water Conservation 67: 321-327. 33. FACTS scheme for training and certification of advisers in plant nutrient management in the UK. https://basis-reg.com/facts/default.aspx 34. Xinhuanet (2014) FACTBOX: China's 11 No.1 central documents on agriculture http://news.xinhuanet.com/english/china/201401/19/c_133057374.htm

Acknowledgements This work was mainly derived from a collaborative China-UK project funded by the UK Foreign and Commonwealth Office and co-funded by the Chinese Ministry of Agriculture. Some aspects were derived from projects funded by the Chinese Academy of Sciences and the UK Biotechnology and Biological Sciences Research Council (BBSRC) through grant-aided support to Rothamsted Research.

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Agroecosystem management in arid areas under climate change: Experiences from the Semiarid Loess Plateau, China Dr Rui-Ying Guo, Professor Feng-Min Li* State Key Laboratory of Grassland Agro-ecosystems, Institute of Arid Agroecology, School of Life Sciences, Lanzhou University, Lanzhou 730000 China. Corresponding author: Feng-Min Li, E-mail: fml@lzu.edu.cn Summary The Loess Plateau is the cradle of ancient Chinese civilization and a place where dryland agriculture originated; it is also one of the worldâ&#x20AC;&#x2122;s most vulnerable ecological systems with the most serious soil erosion problems. The plateau has supported a population of more than 100 million and over 70% of which are rural and are relatively weak. Dryland agriculture has played a key role in providing sufficient food for the inhabitants, as well as , environmental conservation and economic development of the Plateau over the history. It is now facing a considerable challenge from climate change with drier and warmer environment. In order to reverse the serious ecological degradations, especially the significant water loss and soil erosion, the Chinese Government initiated a series of major ecological engineering projects to control the environment. The four significant ecological engineering included 1) a terracing system as a vital tool for agricultural production; 2) a check dam system, constructed in loess gullies to block and collect sediment to prevent its loss to downstream and for cropland improvement; 3) an integrated small watershed control system including dryland farming techniques, water and soil conservation system, and animal husbandry; and 4) the Grain-forâ&#x20AC;&#x201C;Green project in the plateau, returning slope croplands to grassland or forest to increase vegetation coverage and control water loss and soil erosion since 2000. Rainwater harvesting technologies in various forms are becoming the central dryland farming model to improve the efficient use of precipitation, which includes limited irrigation system and ridge-furrow mulching technologies. The grain yield and local farmer income have been increasing rapidly since 2000 due to the efficient rainwater use technologies, especially in recent 5 years. The increasing migration of rural residents to cities for jobs, with rapid urbanization in the recent decades, has alleviated the population pressure in rural areas. With less cropland needed to produce food for the residents, greater amounts of cropland have been returned to grassland or natural vegetation. Therefore, dryland farming technologies, and urbanization indirectly, have benefited the sustainability of the semiarid Loess Plateau. Key words Dryland agriculture, Loess Plateau, low cost, climate change, sustainable development

Abbreviations

RFMTs ridge-furrow mulching technologies; RFRRH ridgeâ&#x20AC;&#x201C;furrow rainwater-harvesting system; LPR Loess Plateau Region; NH Northern Hemisphere

Glossary Isohyets: This refers to a line drawn on a map connecting points that receive

Introduction

he Loess Plateau in China is one of regions where dryland agriculture originated to meet the food requirements of a growing population (1). It is one of the areas with serious soil erosion, which is closely related to the extensive operation of dryland agriculture. Thousands of years ago, the main landforms of the Loess Plateau were expansive flat plateaus with few gullies, and where the forest

equal amounts of rainfall. Orogeny: This refers to forces and events leading to a large structural

deformation of the Earth's lithosphere (crust and uppermost mantle) due to the engagement of tectonic plates.

cover was up to 53% (2-6). With population growth, large areas of natural vegetation (forest, shrub and grassland) had to be converted to cultivation to increase grain production, and eroded sloping areas increased greatly. Forest coverage was reduced from over 50% about 2000 years ago to 33% about 1500 years ago and then to 6.1% by 1949 (3). Soil erosion accelerated as a result of the loss of nature vegetation. For a long period, agricultural production of the Plateau was weak

and unstable which, together with population increase, in caused food shortages and impoverishment of the people. Since the founding of the P R China in 1949, the Central Government has made unremitting efforts, promulgating a series of policies and measures to boost local restoration of degraded ecosystems and improve the livelihoods of the people. In the last decade, with the rapid development of urbanization, a large number of local peasants have migrated to cities for work, which to .

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scientific some extent has reduced rural population pressure. At the same time, the development of low-cost integrated dryland agriculture technology, mainly aims at efficient usage of precipitation, has resulted in significant improvement of agricultural production and the standard of living. The recent Grain for Green Program implemented by the Central Government has led to significant changes in environment and farming production on the Plateau and brought about sustainable ecological restoration and improvement of production (7-8). The conceptual change on the agriculture in the Plateau represents the development in dryland areas of China in the last 60 years, especially the development paradigm of the Loess plateau from productivity to ecological function(9).This paper summarizes agricultural techniques, patterns, and models of the Plateau, describes the evolution of dryland agriculture with the unique characteristics of traditional methods and modern progress and discuss the potential link between dryland agriculture and climate change. It focuses on two aspects: (1) the relationship of environmental management and dryland agriculture of the Loess Plateau of China over the last 60 years and (2) the interaction between ecology and production in seeking sustainable development.

2 Regional backgrounds

2.1 The formation and geomorphology of the Loess Plateau

The Loess Plateau is located on the North central region of China, at latitude 34°~40°, longitude 103°~114°. The plateau stretches over 1,000 km from east to west, and about 700 km from north to south, including the areas west of the Taihang Mountains, Northeast of Tibetan Plateau, north of the Qinling Mountains and south of the Yinshan Mountains. The plateau occupies parts of Shanxi, Shaanxi, Gansu, Qinghai, Ningxia, Inner Mongolia, Henan and some other provinces, a total area of about 640,000km2 (Fig. 1), with the elevation range from 800 to 2,400 m. The formation of the Plateau and the Himalayan orogeny are closely related (10). The Himalayan orogeny led not only to the formation of the Tibetan Plateau, but also to the uplift of the Qinling Mountains, hindering the northwest cold air mass from spreading south, and the southeast warm wet snap from spreading north. The Himalayan orogeny caused the

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Figure 1. Maps showing location and coverage of the Loess Plateau.

gradual strengthening of the northwest wind during the winter, and in Spring it blew dust up to more than 3,000 m in altitude to inland arid desert regions of Central Asia, causing the southeast wind drift. Owing to interference of the southeast monsoon and the barrier and interception of the Qinling Mountains, Liupan Mountains, Lvliang Mountains and Taihang Mountains, the wind was dissipated, depositing its dust along the Yellow River and hence forming the thick loess (11). During the Pleistocene (from about 2,588,000 to 11,700 years ago), the Tibetan Plateau rose to its current height and eventually formed the northwest arid region. As the climate became drier and cooler, Malan loess accumulated more rapidly by wind action, eventually creating the total area of 640,000km2 of loess in northern China and a spectacular Loess Plateau along the middle reaches of the Yellow River (12). Apart from a few rocky mountains, the Loess plateau is covered with thick loess that has a thickness between 50 to 80m, and even up to 150 to 180m. The texture of loess is exquisite and uniform, and the particle size is only 1~10mm. The Plateau is an area of cracked-terrain land, which is mainly divided by ravines and hills. This terrain accounts for about 90% of the area covered by Loess. In the centre of the thickest loess area, there are several relatively flat plateau surfaces between the rivers Jinghe, Luohe, Marin and a few sections of the Puhe. The top surface of the plateau is relatively flat, but some areas are eroded to the valleys with steep sides. The tableland area of Plateau has reduced by soil

erosion to less than 10% of the total area of Loess Plateau (13). 2.2 Climatic characteristics and distribution of dryland farming of the Loess Plateau The southeast monsoon frequents the northwest arid area of the Chinese Loess Plateau (14) and the annual average temperature is 8.8°C (spring 10.0°C; summer 20.9°C; autumn 8.8°C and winter -4.6°C) (13). From 1957 to 2009, the average annual precipitation of the Loess Plateau region was 434 mm (15), with a general trend of more precipitation in the south than in the north, and more in the east than in the west, and a decrease progressively from southeast to northwest (Fig. 2) (15). Most rain falls in the summer (June to August), accounting for 50%~65% of the annual precipitation. Autumn (August to November) accounts for 13%~23%, spring (March to May) accounts for 18%~32% and winter (December to February) is the leastabout 5% (16). The rainy season (May to September) accounts for 78%~92% of the total annual precipitation (16). Arable land of the Loess Plateau covers about 1 458.159 x 104 ha (17). Data for the year of 2008 showed that farmland with slopes greater than 5° accounted for 31.21% of the total cultivated area, in which areas with 5~15° inclines accounted for 42.14%, 15~25° accounted for 19.38%, and >25° for 7.27% (17). The irrigated farmland covers only 25.2% of the total arable land, mainly distributed in west Inner Mongolia and Weihe river plain areas.

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Figure 2. The distribution of mean annual isohyets from nearly 830 mm in the southeast of the Loess Plateau to nearly 100 mm in the northwest in 1957-2009 (Wan et al., 2013)

The rainfed agriculture sector accounts for more than 70% of the cultivated area, mainly distributed in the semi-arid hilly areas with precipitation range 250~550 mm per year. 2.3 Changes in the Climate of the Loess Plateau

Based on the dataset of 224 weather stations on the Loess Plateau, from 1961 to 2010, the average temperature increased significantly (1.91°C/50yr), a greater increase than in the overall northern hemisphere (18). By 2030, the temperatures in Northwest China may be further raised by 1.9~2.3°C (19). However, the overall change in precipitation over the Loess Plateau has not been significant, whereas the precipitation significantly decreased by 47.6 mm per 10-year in the southeast region. According to the rainfall data of 89 weather stations on the Plateau, the precipitation over the entire Plateau fell by 49.1 mm over the 52 years from 1957 to 2009 (Table 1)(15).Spring, summer and autumn exhibited no significant difference in decreasing trend of precipitation, with an average reduction rates of -0.09 mm/a, -0.57 mm/a, -0.19 mm/a,

respectively (16). Since the 2nd century B.C., a trend of increasing drought has been the main climatic observation (20). The frequencies of drought years have consistently increased in the Plateau. In the Sui and the Tang dynasties in the 6-9th century, the proportion of dry years was less than 17%. From then on the probability increased progressively: 27% in the 10th~14th century; 43% in the 15th~17th century; 46% in the 18th century, and >51% since the 1830s (11). An increasing arid climatic trend is bound to have a significant impact on the ecosystem of the Plateau. 2.4 Ecological degradation and poverty in the Loess Plateau

The Plateau is the cradle of ancient Chinese civilization and is one of the world’s most vulnerable ecological environments. The area of soil erosion covers 45.4x104km2 and accounts for 60% of the total Plateau area (of which water erosion covers 337,000 km2, and wind erosion 117,000 km2) (21). The annual loss of soil is estimated a to be 2,000 - 2,500 tons km-2 (22). The main reasons for the soil erosion on the Loess Plateau are drought, heavy

Table 1. The variations in annual precipitation (mm) in different decades across the Loess Plateau, China (Wan et al., 2013).

rain in the summer, steep terrain, loose soil and sparse vegetation (23). In this environmental context, overexploitation and unsustainable agricultural practices included by population growth, such as farming on steep slopes, deforestation, overgrazing, has led to severe ecological degradation. The lost in ecological function of water conservation has led to further erosion (6, 23) and decrease of fertility (2425). According to the Loess Plateau forest distribution map in different historical periods, the coverage of forest declined from 53% (770B.C. ~221B.C.) to 42% (221B.C. ~A.D.8), to 32% (A.D.618~A.D.279) and to 4% (A.D.1386~A.D.1911) (26). Some species disappeared with the destruction of vegetation by human activity over nearly 600 years (27). Ecological degradation exacerbated the impoverishment of people living in the Plateau. According to 2008 statistics, the total population of the Plateau was 108 million, of which the rural population was 73.33 million (17). The population density of the Plateau was 167 people per square kilometer, equivalent to 1.229 times of the national average. The GNP of the area was 1.85 trillion RMB, and rural per capita net income was 3,196 RMB (17). In 2001, the State Council approved a national poverty alleviation and development plan for 592 counties, of which the Loess Plateau region accounted for 115 counties (17). In order to survive, people have to reclaim land, and as a consequence, enter a vicious cycle of ‘the poorer, the more cultivated; the more cultivated and the poorer.’ Therefore, how to reduce soil erosion, and improve the quality of soil and environment, is a task that must be confronted and solved in the Plateau.

3 Four ecological engineering constructions on the Loess Plateau Residents and governments have made tremendous efforts to reduce soil erosion in the Plateau region, promote ecosystem restoration and reconstruction, and promote a comprehensive development of agriculture, forestry and animal husbandry. Through an accumulated wealth of experience, the major ecological projects include terracing, construction of a check dam, small watershed management, and Grain for Green

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Figure 3. Diagrammatic map of four types of terrace in the Loess Plateau

project (Returning farmland to forest and grass). These projects and valuable experience have played important roles in promoting sustainable development in the region. 3.1 Terrace

Terrace is a kind of farmland built on a hill, which in general is divided into four types in the Plateau, namely sloping terrace, interval terrace, flat terrace and back-slope terrace (Fig. 3) (28). Terrace in the watershed of the Yellow river has a long history. There is terraces dating documented and verifiable, back to the Ming and Qing dynasty (1368~1840), and there are hundreds of thousands of terraced hectares of historical legacy. After the

founding of New China, governments of all levels have paid attention to the construction of terrace over the last 60 years. Before 1958, the terrace was mainly built on the hill; after 1958, mainly constructed as level terrace, and since 1990, mechanized level terracing has been adopted and construction efficiency was greatly improved (29). The statistics of 2008 showed that the area of terraced landscape on the Plateau covered325.6x104 ha, accounting for 22.33% of the total arable land area (1458.159x104 ha) in the Plateau (17), and it is expected that over the period of 2010~2030, 260.8x104 ha of land will be terraced (17).

Terracing is the primary step for farming on the Plateau. Terraced slope can be altered to reduce the slope length and increase rainfall infiltration rate, enhancing soil water storage, improving the efficiency of water and nutrient use (4, 6, 30-32). From 1951 to 1995, retention of water of the Yellow River basin by terrace reached 19 billion m3, which accounting for 23.4% of the total storage capacity of soil and water conservation (81.27 billion m3) (29). A large number of tests have shown that terraced water efficiency and soil conservation benefit could have attained 86.7% and 87.7%, respectively (Table 2). Effects of water and soil conservation by terraces have a very close relation with the precipitation. For example, when the single rainfall integrated parameters, annual rainfall and flood flow rainfall were less than 2010 mm2/min, 350 mm and 125 mm, the benefits of the soil and water conservation by the terraces could reach 100% (33-34). For example, when the rainfall synthesis parameter PI, rainfall in flood period, annual rainfall of runoff generation were less than 20.0 mm2/min, 350 mm and 125 mm, respectively, the benefits of the soil and water conservation by the terraces could reach 100% (34). However, the conservation benefits of terraces would be lower when rainfalls were larger.

Table 2. The benefits of soil and water conservation of flat terrace on the Loess Plateau (Wu et al., 2004).

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Table 3. Crop production and increases compared with yields in sloping fields >10o on terraced land constructed in different years (Liu et al., 2011).

Terrace level also affects the quality of soil and water conservation. The terraces on the Plateau may be divided into three quality categories according to their soil and water conservation benefits (35). Category 1 is best quality, in which soil and water conservation benefits are 87% and 90%, respectively; Category 2 is good quality, the both benefits are 82% and 85%, respectively; Category 3 is poor quality with both the benefits of 76% and 78%, respectively (35). The construction of terraces greatly increased crop yields (Table 3) (36,37,38). Terraces not only increase conventional crop yields but also accelerate the development of cash crops, including vegetable, fruit and potato production on the Plateau, and increase per capita income (Fig. 4) (37). Due to agricultural development on terraces, the population carrying capacity of the Plateau also increased from the 148 people/km2 to 374 people/km2 (37). The construction of terraces also provides convenient conditions for the optimization of farming technology and has a profound impact on regional

sustainable development. 3.2 Check dams in the Loess Plateau

A check dam is considered the most effective way to reduce soil erosion in the river (39-40). Soil erosion in the Plateau is mainly derived from the slopes and river banks. In the loess gully region, the proportion of the total sediment deposited from the river banks is 90%, i.e. 9 times the amount deposited from the slopes (41-43).The check dam blocks the transport of sediment to the downstream area and collecting the sediment. The check dam raises the base level of slope’s bottom, reduces the soil erosion, and effectively prevents the soil of cutting. The check dam prevents the gully bank’s erosion. Check dams block the sediments efflux from slopes area to the gully area (44). Dams have a history similar to that of the terraces, dating to the Ming Dynasty. Renowned water resource expert, Li Yizhi, who advocated the ‘Gouxu’theory to manage the Yellow River, and introduced check dams as part of a strategy to govern the River. In 1945, China invested in the first

Figure 4. Farmers income per capita (Yuan) during 1985-2005 in Zhuanglang County, Gansu Province, China. (Construction of large-scale terracing across the entire Zhuanglang County started in the 1960s, and in 1998 almost the entire county was terraced. The terraced fields accounted for 95% of the total arable land) (Liu et al., 2011).

‘government-run’ check dam (29). Since 1949, the construction of check dams has reduced the water and soil loss of the Plateau (45-46). In the last 50 years of the 20th century, more than one hundred thousand of check dams have been built in the Plateau (5). In 1983, the ‘Key conservation of soil and water in the Gullies’ project conducted a three-year experiment to develop appropriate planning, and technical specifications and regulations (Table 4) (44). Since the implementation of this ‘Key Gully Plan’ in 1986, 1,118 of check dams were established since then till 1999 on the Plateau (45). However, it is expected to take another 100 years to complete the remaining construction of approximately 130,000 check dams (5). Dams constructed in the Yellow River region (1951~1952) held back 9.6 billion m3 of water accounting for 11.8% of the total impeded by conservation measures. The effect of intercepted sediment and reduced runoff is closely related to the height of each check dam. According to the statistics of 4,877 check dams, those with heights of 5~10, 10~15, 15~20, 20~25 and 25~30m, had sediment interception efficiencies of 13.5%, 27.9%, 38.3%, 42.0% and 48.4% respectively, and efficiencies of runoff reduction of 1.97%, 4.63%, 7.26%, 6.37% and 7.73%, respectively (33). Check dams have become a unique characteristic of the Chinese Loess Plateau. They play an important role not only ecologically, but also in grain yield. Dams produce high fertility and soil moisture (5, 47). Grain output is typically increased the by 8~10 fold (5, 41)and even up to 16 fold (48) that of the hilly farmland. Planting around 1 ha of dam is equivalent to planting on 2~3 or 5~6ha of terraced slopes (48).

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Table 4. Scheme for the check-dam systems, including numbers of key projects and check dams in the Loess Plateau (Huang, 2000)

A study of the World Bank Loan Project for Yan River Watershed Management (1994 to 1996) showed that the input rates of dams, terraces, irrigated agricultural land were 3.3, 2.4 and 4.2 times that of hilly land, respectively, while their net benefits were 12.8, 5.1 and 13.2 times that of the inclined land, respectively (29). Although the check dam has a significant role in reducing gully erosion and increasing agricultural production, it is still controversial. Four reasons are for this point. (1) Check dam construction requires a substantial investment in financial and human resources. (2) Due to insufficient funding, the construction quality of a majority of check dams is poor, so the collected sediment is unlikely to prevent flooding and may even exacerbate soil erosion. Owing to this poor quality, following a prolonged drought, in 1977 and 1978 they were subject to frequent rainstorms, and it was estimated that more than 80% of the dams were destroyed (5), leading to fulminant and serious soil erosion. (3) Following dam construction, agricultural production is facing enormous challenges. Because of poor drainage of new farmland near dams, nearly 33.3%~50% of the dams in northern Shaanxi and western Shanxi suffered from salinization, causing grain losses of 50 million kg. (4) The long-term ecological impact and role of this large-scale human check dam’s intervention in the Plateau is unclear (5). Therefore, the large-scale promotion of check dam construction needs careful consideration from engineering, technical and ecological angles for farming. In more recent times during China's economic development, the materials and techniques of check dam construction have been developed considerably and

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can effectively prevent storm erosion. Nevertheless, check dam construction requires a lot of human resources, and it continues to be an enormous financial burden (49). 3.3 Integrated management of small watersheds in the Loess Plateau

The integrated watershed control of soil erosion is a summary of long experience, and lessons learned. Early comprehensive treatment of watersheds was applied in many countries during the 19th century (5052), and proved to be a practical technology which could reduce soil erosion and enhance ecosystem resilience (53). The integrated watershed system is considered a small watershed as a unit, according to the characteristics and patterns of soil erosion, local conditions, farmland fortification, engineering measures taken, plant measures combined with agricultural technical measures, comprehensive management of landscape, farmland, forest and roads, rational use of rainwater and land resources, optimizing structure of agriculture, forestry and animal husbandry (23). There are more than one million small watersheds in Yellow River Region, and each watershed is from a whole geographical unit, where the generation of sediment transport from a small basin. There is a need to consider all of the major factors controlling soil erosion for ‘integrated watersheds’. These include farmland construction, commercial forestry, fuel, protection of woodland planting, soil conservation, adjustment of agricultural structure and needs of local people (23). It combine reduction of soil erosion with local economic growth, applying a variety of effective ecological engineerings (terracing, check dams and soil reservoirs) and

environmental management techniques (contour farming and straw mulch) (5). These measures started in the 1980s, coordinated the ecological restoration and increase of productivity (54). By 2000, these projects have been carried out in more than 5 000 basins (5). The CAS Institute of Soil and Water Conservation and other relevant organizations in Shaanxi Province have built 5 models, and 11 comprehensive management demonstration areas, achieving good economic and social benefits. The total loss of soil in 11 typical watersheds reduced by 50%~90%, and crop yields increased significantly. Nevertheless, the implementation of integrated small watersheds in the Plateau presents problems. First, this project will require substantial external financial, material and human resources (5). Second, there are more than a million small watersheds in the Plateau that has been costly. Thus, although small watershed management in the area has gained remarkable success, it has been too slow to relieve environmental deterioration. Thus, at present the ecological status of the Loess Plateau is still deteriorating overall, despite some ‘partial improvements’ (55). 3.4 Grain for Green project

Grain for Green project is a large ecological engineering aiming at ecological restoration and soil erosion reduction in China (56). According to regulations, the farmland in slope with the gradient >25° for southwest and >15° for northwest in China, respectively, should be replaced with grasses and trees. Farmers participating in the project receive grain, treeing seedlings, grasses seeds and cash as compensation provided by the government (57). The pilot project of Grain for Green was carried out in 1999 in Sichuan, Shaanxi and Gansu provinces, and formal project began from 2002. The project involved 25 provinces and 1897 counties in China. Till now, Grain for Green project is an ecological engineering with strongest policy and became the world's largest ecological engineering (56). Grain for Green project has changed the local employment and income structure (58). For example, in Wuqi County, the proportion of the labor force engaged in the cultivation before the ‘Grain for Green project’ was 87.82% in 1998, fell to 19.16% in 2006 (58).

scientific the people of the Plateau were very poor (42). The Grain-for-Green project provides Government subsidies as a main income source for each farm household but only until 2018. An investigation of livelihoods indicates that 37.2% of farmers may re-cultivate the ‘returning land’ in the Plateau (8). Therefore, improvement of dryland agricultural techniques relates to both regional and China’s food safety, to the livelihood of local people, to the past achievement of Grain-for-Green Project and to the ecological restoration of the Loess Plateau.

Figure 5. The dynamics of total area of cropping land (104 ha), total grain yield (107 kg), grain yield per hectare (102 kg ha-1)and grain yield per capita(kg Hd-1) in the dryland area of Gansu Province (from 1993 to 2011, which included the Yuzhong County, Huining County, Tianshui region, Pingliang region, Qingyang region and Dingxi region) (the data are from Gansu statistical yearbook).

The proportion engaged in animal husbandry raised from 6.3% to 24.6%, but there´s a significant decline in herd sizes, because the grazing leads to higher costs of feeding and raising forage shortages. The main labor reduced from agriculture moved to the relatively high income industries such as building construction, catering, transportation and other nonagricultural industries. After returning farmland, the compensation income becomes the main source of income of local farmers, followed by families operating income and subsidy of returning farmland to forest, the ratio were 48.31%, 27.39% and 24.30%. The grassland area increased 20.3%, the forest area increased by 13.786 times (58). The main three factors guarantee the successful implementation of Grain for Green Project are. The first one is government's high-handed policy, there’s a huge investment for this project. The second is the rapid development of China's economy and urbanization; this provides an opportunity for farmers who migrate to cities, they can get a higher income than farming at home, the land is no longer their main income source. The third is great progress of dryland agriculture technology; it provide a guarantee to achieve enough food and higher economic benefit in limited lands (59). According to the project plan, the government subsidies of Grain for Green project will end in 2018 (60). Thus, although the sustainability of Grain for Green Project remains to be seen, but on the whole, it ought to help keeping the vegetation coverage, rural industrial structure adjustment, in order to

promote the ecosystem reconstruction and sustainable development (60).

4 The development of dryland agriculture in the Loess Plateau 4.1 The significance of dryland agriculture

Dryland Agriculture is the main system, charged with the task of self-sufficiency in the Plateau (42, 61). Since China's central government implemented the grain-for-green project in the plateau in 1999, the cultivated land area declined by 10.1% from 1996 to 2007, including a dramatic decline of 15.15% from 1996 to 2003 (62). From 2003 to 2007, the cultivated area increased by 5.95% compared with that in 2003. Between 1996 and 2007 grain productivity decreased by 3.76%, a lesser decline than that of the cultivated area (62). A dramatic decrease of total grain production in Loess Plateau was about 8.73% from 1996 to 2003, whereas between 2003 and 2007, grain production increased by 5.45% over that in 2003, owing to an increase in the area cultivated (62). In Gansu province, following the Grainfor–Green project, total grain yield, the grain yield per unit area and the grain yield per capita all increased fairly uniformly (Fig. 5). The improvement of dryland tillage techniques increased output per unit area (63-69). Despite China’s grain production policy, it was planned to restore the ecology of western China while the price of grain fell (70). However, any change in grain production through implementation the policy should include local self-sufficiency (62), as

4.2 The development of dryland agricultural techniques in the Loess Plateau

The key to dryland agriculture is utilizing limited rainfall efficiently (71). In a typical semi-arid region of the Plateau, the precipitation over farmland distributes as follows: evaporation loses 50%~60% of rainfall; plant transpiration used 30%~40% rainfall; and about 10% rainfall lost as runoff or by other routes (72). The annual precipitation over the entire Plateau is about 3000 billion m3, which is equivalent to five times the amount needed in this area (72). Water-harvesting eco-agriculture is the main tillage mode to increase the efficiency of use of precipitation in the semiarid Loess plateau (73). A series of tillage techniques are designed for rainfall harvesting at minimal cost. These techniques are successful examples for improving grain productivity in dryland of developing countries (74). The system is based on traditional terraces and horizontal trenches to gather precipitation. Either the rainwater is gathered into a underground cistern to supplement irrigation at the critical period of crop growth, or the rainwater is drained into the crop planting zone by the rainwater harvesting surface, e.g. a plastic film mulched ridge-furrow system, which can enhance the water supply in plant growth zone (75-77). The technique can improve rainfall utilization efficiency in dryland. 4.2.1 Limited (supplementary) irrigation technique of the dryland Loess Plateau

Supplementary irrigation was mainly due to the farmer’s requirement of low cost and a growing shortage of ground water resource (78). Limited irrigation achieved good results in the Midwest Great Plains in the U.S., where the rainfall is about 480mm annually.

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scientific Experiments showed that continuous cultivation of dryland is possible when limited irrigation (about 150mm) is carried out at the critical stage of a crop’s water requirement. Grain production could be increased by over 60%, and water efficiency doubled compared with an adequate irrigation treatment (78). In China, according to the local situation, some expert defined the limited irrigation as ‘according to the amount of available water resource in local area and water requirement of local crop, the manager conduct the lowest water supplying based on the natural rainfall condition’ (72). In the hilly region of the Plateau, the irrigation water relies mainly on rainfall. Underground water tanks can be established to collect rain and provide supplementary irrigation at the critical stage of crop growth. In Gansu province, a typical semiarid region of the plateau, a so-called ‘121’ rainwater harvesting project had been initiated by the local government in 1995. The government supported the construction by each household, one area for water collection, two storage areas and one to plant cash crops (71). This project has successfully provided drinking water for 1.3 million people and their 1.18 million livestock. In 1997~1998 a rainwater catchment and irrigation project was instituted to provide supplemental irrigation water with a highly efficient method. This produced higher crop yields (79-80) and full utilization of natural rainfall to support dryland agricultural with water-saving irrigation (from 1997 to

2010). The system of water-harvesting has been greatly improved developed a new water-tank system with low cost specifically for the semiarid Loess Plateau (81). Meanwhile, the waterharvesting technique was used together with micro-irrigation, increasing the crop’s water use efficiency (34, 82). In addition, a simple supplemental irrigation, with low cost such as wet sowing and hole irrigation with mulching, could further improve the crop water use efficiency (71). Nevertheless, limited irrigation could not be used widely for grain crops in the semiarid Plateau, because of the small quantities of rain collected and the high cost of establishing the system (80). In order to benefit from the cost of an increase in supply of unavailable water, it is recommended that supplemental irrigation should be used mainly for cash crops, e.g. potatoes and other vegetables. 4.2.2 Ridge-furrow mulching technologies in the Loess Plateau

Ridge-furrow mulching technologies (RFMTs) were proposed and innovated by a local research worker in Gansu province (83). In the central area of the Plateau in Gansu province, the yields of wheat, oat, potato and pea are low and unstable (the spring wheat yield is 2,250~3,000 kg per ha). In order to improve farmers’ livelihoods, RFMTS are used to extend planting of maize in the semi-arid Plateau. These RFWHS are based on the concept of gathering

Figure 6. Sectional view in ridge–furrow rainwater-harvesting system (RFRRH).

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and using rain in-situ (Fig 7). By modifying the micro-topography of farmland, limited rainfall is retained in the furrow- the location of the crop root zone. Rain is redistributed in space at the field level (84). It is an innovative technique for boosting crop productivity in semiarid rain-fed environments (85).A field is cultivated with a wide ridge and a narrow ridge (‘double ridge’) before spring or autumn sowing, and then the entire soil surface is covered by plastic film. The seeds are sowed in the furrow between broad and narrow ridges (Fig.6). Maize grain yield on RFMTS could reach 7 500~9 000 kg ha-1, higher than other traditional crops, e.g. wheat, oat, pea and maize without film covering (86). RFMTS increase maize yield by 30%~90% compared with normal cultivation (86), and wheat yield by 100%~150% (75). In the cooler region of northwest China, maize cannot attain reproductive development in time to produce a viable cob, but with a plastic film mulching the crop can be planted earlier and it emerges earlier so that reproduction is not compromised (67, 86-87). The increased quantity of maize straw assists local livestock breeding (88) and reduces grazing pressure on natural grassland. As a consequence of the tremendous increase in yield, the areas over which RFMTS are used has gradually increased, and they have been adopted for crops such as wheat and potato (89-91).

scientific

Table 5. The effect of plastic film residue into soil on maize production (kg/ha) (unpublished data from Li’s group of Lanzhou University), modeling after 0 to 60 years by F0, F10, F30, F60, measured during two years (2012, 2013)

From 2008, use of RFMTS has been extended by the Ministry of Agriculture to Qinghai, Inner Mongolia, Ningxia, Shaanxi and Shanxi provinces. Through long-term research and practice, the best ratio of ridge, furrow and plastic covering time has been determined for various climates, soil types and crop water requirements (84, 92-93). Increased yields with RFMTS should be attributed to three factors: (1) inhibiting water evaporation from the soil surface and increasing soil water content during critical stages of crop growth by the plastic film mulching (67,83,85); (2) increasing soil temperature, and hence accelerating seedling emergence and early growth in cooler locations (85, 94) and (3) improving soil nutrient availability, especially nitrogen (81). RFMTS contribute to rain use and crop yield where the annual precipitation is in the range of 230~440 mm (95). RFMTS increase crop yield but with excessive soil utilization (96). As a result of increased soil temperature and moisture content, soil microbial C and N biomass, soil enzyme activity, soil respiration rate and nitrogen mineralization rate are all increased (92, 97-98). Thus, Li et al (99) reported that in an upland rice system soil organic matter and total N could be reduced by 8.3%~24.5% and 5.0%~22.0%, respectively, with film covering in contrast to that without the film. Therefore, it is proposed that the application of RFMTS should be combined with increasing soil organic matter content (100). The ‘white’ pollution (plastic mulching waste) has led to dispute in dryland application of RFMTS. A few studies have focused on the effect of plastic film residues on crop yield and soil quality. It is estimated that about 45kg ha-1 yr-1 of plastic film residues occur. We conducted a pilot field experiment with 10-year, 30-year and 60-year accumulative residue of plastic film in

Zhonglianchuan and Xiaguanying, Yuzhong County, Gansu province. The corresponding amount of plastic film residue was 450kg ha-1, 1,350 kg ha-1 and 2,700 kg ha-1, respectively. The film was shredded and incorporated into the field. The preliminary result showed that this residue has no significant influence on maize yield in contrast with the treatment without film incorporation (Table 5, unpublished data). But further research should be conducted on the effect of film residue on crop yield and soil quality over extended periods.

5 Conclusions The two key driving forces of ecological degradation in semi-arid areas of the world are nothing more than climate change and unsuitable human activities. Climate change has resulted in drier and warmer in the Loess Plateau. This leads to a decline in vegetation and then to a series of environmental issues. Unsuitable human activities implies that in order to increase food production or land income for ridding the local poverty, the people have to cultivate and over-graze more land, which results in damage to sustainability of the ecosystem, and then in its further degradation. Ecological degradation enlarges the gap between demands of local people and ecosystem services. This leads to further aggravated predatory land reclamation, and a vicious cycle of ecological degradation occurs. The primary way to overcome the ecological problems is to increase unit land productivity so that a fewer area of cultivated land meets the needs of the local population. This procedure alleviates the ecological pressure, providing the space for its ecological restoration. The Loess Plateau Region is a unique area with an historic accumulation of loess. Excess land reclamation and

over-grazing for food production resulted in an extensive environmental degradation, causing widespread poverty that has plagued the local government and people for many decades. Since P R China was founded in 1949, the Central Government and social organizations have paid much more input to the development of the plateau, and taken a series of measures including the application of ecological engineering and improvement of agricultural techniques. However, this region was still impoverished and ecological deterioration continued before the turn of the new century. From the year 2000, dryland farming productivity on the plateau has increased significantly and livelihood greatly improved with the farming development of new techniques of high rainfall use efficiency. Meanwhile, the progress of China’s economy has promoted a rapid urbanization and more and more local young residents move to cities to find jobs. Both movements are the main driving forces to land use change and ecological restoration. The local people can use less land than before to feed themselves and improve their living standard. A greater area has been returned to grassland or natural vegetation. The area of vegetation has increased while the climate has become drier and warmer. The change of the pattern of land use shows a new promise for the Loess Plateau, and it contributes to the strategy of “large land for ecological restoration and small land for farming production” in the Loess Plateau. However, there is still a long way to go for dryland farming development of the Plateau owing to uncertainty and future challenges of climate changes. More research and further positive measures should be taken to establish new complex ecosystems and realize the harmony of production and environment in the context of climate change.

Acknowledgement The authors are grateful to Dr Frape David for his patient advices and to Dr Pete Falloon for his valuable commentary. This research was supported by program of Chinese Ministry of Science and Technology (2011BAD29B04), MOST International Sci-Tech Cooperation Program (2010DFA32790), ‘111’ Project (B0751), and the Fundamental Research Funds for the Central Universities (lzujbky-2010-k02, 860974).

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Rice terraces. Yunnan, China plastic film mulching periods on the soil nitrogen availability in semiarid areas. Acta Ecologica Sinica. 21(9): 1521-1526. 80. Gan, Y. T., Kadambot H. M., Siddique, Turner, N. C., Li, X. G., Niu, J. Y., Yang, C., Liu, L. P., Chai, Q. (2013). Ridge-Furrow Mulching Systems—An Innovative Technique for Boosting Crop Productivity in Semiarid Rain-Fed Environments. Advances in Agronomy. 118: 429–476. 81. Hai, L. (2010). Effects of plastic-film mulching on maize yields and soil quality in the semi-arid Loess Plateau of China. PhD thesis, Lanzhou University. 82. Jin, S. L., Zhou, L. M., Li, F. M., Zhang, G. Q. (2010). Effect of double ridges mulched with wide plastic film on soil water, soil temperature and yield of corn in semiarid Loess plateau of China. Agricultural Research in the Arid Areas. 28(2): 28-33. 83. Zhang, W. S., Li, F. M., Xiong, Y. C., Xia, Q. (2012). Econometric analysis of the determinants of adoption of raising sheep in folds by farmers in the semiarid Loess Plateau of China. Ecological Economics. 74:145-152. 84. Wang, Q., Zhang, E. H., Li, F. M. (2004a). Runoff efficiency and soil water comparison of plastic-covered ridge and ridge with compacted soil at different rainfall harvesting stages in semiarid area. Acta Eologica Sinica. 24(8): 18161819. 85. Wang, X-L., Li, F-M., Jia, Y., Shi, W-Q. (2005c). Increasing potato yields with additional water and increased soil temperature. Agricultural Water Management. 78(3): 181- 194 86. Tian, Y., Li, F. M., Liu, X. L. (2007). Effect of different ridge-furrow planting patterns of potato on soil evaporation in semiarid area. Chinese Journal of Applied Ecology. 18(4): 795-800. 87. Song, Q. H., Li, F. M., Liu, H. S., Wang, J., Li, S. Q. (2003). Effect of plastic film mulching on soil microbial biomass in spring wheat field in semiarid loess area. Chinese Journal of Applied Ecology. 14(9): 1512-1516. 88. Wang, Q., Zhang, E. H., Li, F. M., Wang, X. L. (2005b). Optimum ratio of ridge to furrow for planting potato in micro-water harvesting system in semiarid areas. Transactions of the CSAE. 21(1): 38-41. 89. Wang, Q., Zhang, E. H., Li, F. M., Li, F. R., Xu, C. L. (2005a). Effect of generation characters of mini-size water collection by ride sand furrows in semiarid area of Loess plateau and related potato planting techniques. Chinese Journal of Ecology. 24(11): 1283-1286.

© silver-john – fotolia.com 90. Ren, X., Chen, X., Jia, Z. (2009). Ridge and furrow method of rainfall concentration for fertilizer use efficiency in farmland under semiarid conditions. Applied Engineering in Agriculture. 25: 905–913. 91. Wang, J., Li, F. M., Jia, Y., Li, S. Q., Song, Q. H. (2004c). Effects of plastic film mulching and presowing irrigation on yield formation of spring wheat. Journal of Desert Research. 24(1): 77-82. 92. Li, F-M., Song, Q-H., Hao, J-H., Jjemba, P. K., Shi, Y-C. (2004b). Dynamics of soil microbial biomass C and soil fertility in cropland mulched with plastic film in a semiarid agro-ecosystem. Soil Biology and Biochemistry. 36(11): 1893-1902. 93. Bu, Y-S., Miao, G-Y., Zhou, N-J., Shao, H-L., Wang, J-C. (2006). Analysis and comparison of the effects of plastic film mulching and straw mulching on soil fertility. Scientia Agricultura Sinica. 39(5): 1069-1075. 94. Li, X., Shi, H. B., Chen, M. J. (2007). Effects of the supplemental irrigation of harvested rainwater on the growth and yield of maize. Transactions of the CSAE. 23(4): 34-38. 95. Zhou, L. M., Jin, S. L., Liu, C. A., Xiong, Y. C., Si, J. T., Li, X. G., Gan, Y. T., Li, F. M. (2012b). Ridge-furrow and plastic- mulching tillage enhances maize-soil interactions: opportunities and challenges in a semiarid agroecosystem. Field Crops Research. 126: 181-188. 96. 1.Wang, J., Li, F. M., Jia, Y., Li, S. Q., Song, Q. H. (2004). Effects of plastic film mulching and presowing irrigation on yield formation of spring wheat. Journal of Desert Research. 24(1): 77-82. 97. Li, F-M., Song, Q-H., Hao, J-H., Jjemba, P. K., Shi, Y-C. (2004). Dynamics of soil microbial biomass C and soil fertility in cropland mulched with plastic film in a semiarid agro-ecosystem. Soil Biology and Biochemistry. 36(11): 1893-1902. 98. Bu, Y-S., Miao, G-Y., Zhou, N-J., Shao, H-L., Wang, J-C. (2006). Analysis and comparison of the effects of plastic film mulching and straw mulching on soil fertility. Scientia Agricultura Sinica. 39(5): 1069-1075. 99. Li, X., Shi, H. B., Chen, M. J. (2007). Effects of the supplemental irrigation of harvested rainwater on the growth and yield of maize. Transactions of the CSAE. 23(4): 34-38. 100. Zhou, L. M., Jin, S. L., Liu, C. A., Xiong, Y. C., Si, J. T., Li, X. G., Gan, Y. T., Li, F. M. (2012). Ridge-furrow and plastic- mulching tillage enhances maize-soil interactions: opportunities and challenges in a semiarid agroecosystem. Field Crops Research. 126: 181-188.

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Interactions between orogeny, climate and land use in the Semiarid Loess Plateau, China Dr Pete Falloon Met Office Hadley Centre, Fitzroy Road, Exeter, EX1 3PB pete.falloon@metoffice.gov.uk Glossary Land cover change: the replacement of

one land cover type by another, e.g., due to expansion of croplands, deforestation, or a change in urban extent. Land management change: a change

uo and Li (2014) present a fascinating study of the history of agriculture in the Chinese Semiarid Loess plateau, and suggestions for sustainable future management options. The region, and Guo and Li’s study are particularly interesting from a climatological perspective because of the two-way interactions between orogeny and land use and the climate in this region. Himalayan uplift created the Qinling Mountains, with several beneficial climatic effects. The mountains prevented the Northwest cold snap from spreading southwards into the Loess plateau, and also prevented the warm snap from the Southeast spreading further north, ensuring a more temperate climate in the region. Wind drift from the Southeast blew dust towards the region in spring, while the Southeast Monsoon and the barrier effect of the mountains mean that the winds deposited their dust along the Yellow River basin, resulting in thick loess deposits. The existence of these thick loess deposits, and the more moderate climate, were foundations for fertile rain-fed agriculture in the region. However, subsequent agricultural expansion in the region also had a long-term negative impact on productivity, through knock-on effects of severe deforestation. The Loess plateau was 50% forest 2000 years ago, but only 6.1% of forest cover remained by 1949, leading to significant soil erosion. Since 1949, a programme to restore degraded ecosystems attempted to reverse this trend. In the last decade rapid

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in how humans treat vegetation, soil, and water for a specific purpose – for instance the use of fertilizers and pesticides, irrigation, use of introduced grass species for pasture, the tree species used in reforestation and

livestock movement. Albedo: is the fraction of solar energy (shortwave radiation) reflected from the Earth back into space. It is a measure of the reflectivity of the earth’s surface.

urbanization has also led to lower population pressures in the region, drawing people from rural areas to regional centres. The “Grain for Green” initiative meant that cultivated land in the region declined by approximately 15% from 1996-2003 although there was been a small increase between 2003 and 2007. The current focus on agriculture has been on low-cost dryland technologies to make more efficient use of limited precipitation. This has been particularly important given a long-term trend towards drought, and heavy summer rains. It is estimated that 50-60% of farmland precipitation is lost by evaporation, 30-40% through plant transpiration and 10% through runoff. (Some is retained, especially by green crops.)There is limited potential for widespread irrigation in the region. Timing water supply to meet crop needs is a critical issue in the Loess plateau. Land management in the region, and the key to a sustainable, productive future therefore focuses on integrated watershed management and water harvesting techniques. These include terracing and check dams to reduce soil and water loss, and increase fertility and soil moisture, and ridge furrow mulching with plastic films; although the latter may have some negative impacts through lower soil C and N contents due to warmer, wetter soils. The human-driven changes in land cover (LCC1) and land management (LMC2) in the Loess plateau over the last 2000 years may have led to impacts on climate themselves (e.g. Betts et al., 2007; Raddatz, 2007; Pongratz et al., 2010), potentially by

altering biogeochemical processes (e.g. C and N cycling) and biophysical effects (such as surface albedo3, surface roughness and evapotranspiration). Deforestation to agriculture or grassland (e.g. Davin and De NobletDucoudre, 2010; Lee et al., 2011) tends to reduce evapotranspiration rates, with a warming effect on climate. The brighter crops have a higher albedo, potentially cooling the climate. A further significant impact of agricultural expansion is during winter and spring in climates where snow cover is significant, as the bare soil allows a much brighter, snow covered surface with higher albedo than the forested regions, to have an additional cooling impact. Overall, deforestation in cool regions may cool local climate because the effect of increased surface albedo tends to be dominant, while increases in cool-region forest area may have the opposite effect (Falloon et al. 2012). Outside the tropics, impacts of LCC and LMC on precipitation are often less pronounced (Falloon et al. 2012). Recent climate modelling studies have indicated that warming resulting from large-scale mid-and-high latitude afforestation may be altered by enhanced transpiration (Swann et al., 2010) and water vapour export (Swann et al., 2011), triggerring further feedbacks and changes to circulation patterns. For instance, large-scale afforestation in Northern Hemisphere mid-latitudes (45o to 60oN) may warm the Northern Hemisphere and alter the Hadley circulation leading to a northward displacement of tropical rain bands (Swann et al. 2011).

scientific Swann et al. (2010) found that afforestation with deciduous trees at Northern Hemisphere high latitudes led to stronger climate impacts from greater transpiration compared to the effect of albedo changes; warming from increases in atmospheric water vapour content melted sea ice, triggering a positive feedback via ocean albedo and evaporation. It is therefore possible that historic deforestation in the Loess plateau may have cooled the local climate, depending on the balance between albedo and evapo-transpiration effects, although such impacts may be difficult to detect in observational climate records. The more subtle recent changes in LMC to prevent soil and water loss and preserve fertility may also have effects on climate. Although the climate effects of LCC have been much more widely studied than those of LMC, Luyssaert et al (2014) show that LMC may have impacts on surface

Shanxi Loess Plateau road

temperature of a similar magnitude to those of LCC. The story of the Loess plateau, and future prospects described by Li (2014) tell us that the key to future sustainable food production in challenging environments is to harness our knowledge of how land use, soil, water, and climate interact with each other (Falloon & Betts, 2010) to make the best use of limited natural resources.

References Davin, E. L. and de Noblet-Ducoudre, N.: Climatic impact of global-scale deforestation: radiative versus non-radiative processes, J. Climate, 23, 97–112, doi:10.1175/2009JCLI3102.1, 2010. Falloon, P. D., Dankers, R., Betts, R. A., Jones, C. D., Booth, B. B. B., and Lambert, F. H.: Role of vegetation change in future climate under the A1B scenario and a climate stabilisation scenario, using the HadCM3C Earth system model, Biogeosciences, 9, 4739-4756, doi:10.5194/bg-94739-2012, 2012. Falloon, P., and Betts, R. (2010). Climate impacts

on European agriculture and water management in the context of adaptation and mitigation: the importance of an integrated approach. Science of the Total Environment 408(23): 5667-5687. Lee, X., Goulden, M. L., Hollinger, D. Y., Barr, A., Black, T. A., Bohrer, G., Bracho, R., Drake, B., Goldstein, A., Gu, L., Katul, G., Kolb, T., Law, B. E., Margolis, H., Meyers, T., Monson, R., Munger, W., Oren, R., Paw U, K. T., Richardson, A. D., Schmid, H. P., Staebler, R., Wofsy, S., and Zhao, L.: Observed increase in local cooling effect of deforestation at higher latitudes, Nature, 479, 384–387, 2011. Li, F (2014) Climate change and agro-ecosystem management in arid areas: experiences from the Semiarid Loess Plateau, World Agriculture (in press) Luyssaert S et al. (2014), Land management and land-cover change have impacts of similar magnitude on surface temperature, Nature Climate Change, doi:10.1038/nclimate2196 Swann, A. L., Fung, I. Y., Levis, S., Bonan, G., and Doney, S.: Changes in Arctic vegetation induce high-latitude warming through the greenhouse effect. P. Natl. Acad. Sci. USA, 107, 1295–1300, doi:10.1073/pnas.0913846107 , 2010. Swann, A. L. S., Fung, I. Y., and Chiang, J. C. H.: Mid-latitude afforestation shifts general circulation and tropical precipitation, PNAS, 109, 712–716, doi:10.1073/pnas.1116706108 , 2011.

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Plastic-film mulch in Chinese agriculture: Importance and problems Professor Yan Changrong1, Dr. He Wenqing1*, Professor Neil C. Turner2, Dr. Liu Enke1, Liu Qin1, Liu Shuang1 1 Institute of Environment and Sustainable Development in Agriculture, CAAS/Key Laboratory of Dryland Farming Agriculture, MOA, No.12 South Street Zhongguancun, Beijing, 100081, P.R. China; 2The UWA Institute of Agriculture and Centre for Plant Genetics and Breeding, M080, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia Tel:86-10-82106018; Fax:86-10-82106018 E-mail:yancr@ieda.org.cn; yanchangrong@caas.cn Summary Plastic-film mulch is widely used to increase the productivity of crops, vegetables and fruit trees in cold and arid or semiarid regions of China. Use increased from 6000 t, covering 0.12 million ha, in 1982, to 1.2 million t, covering almost 20 million ha, in 2011. The thin (4-8 Âľm) polyethylene film used in China is slow to degrade, easily damaged, difficult to reuse for a second season and difficult to remove. Residual plastic in the top 0.3 m soil layer is now estimated to vary from 72 to 260 kg/ha, depending on number of years use, percentage of ground covered and film thickness. Research results showed that plant growth was affected when residual plastic exceeded 37.5 kg/ha in the soil; the emergence of winter wheat seedling decreased by 25% and the tiller number decreased by 17%. Cotton yields were reduced by 4%, 8%, 12% and 19%, respectively when the amount of residual plastic in the soil was 80, 170, 280 and 370 kg/ha. Use of photo- and biodegradable plastics is currently considered to be too expensive for agricultural use in China, but we suggested that use of thicker (15 Âľm) and stronger film that can be reused for two or more years, together with planters that can collect the residual plastic while (planting) sowing, the seeder should be developed. Keywords plastic residues, soil pollution, yield decline, degradable plastic film, China

1. The application of plastic-film mulch in agriculture

he use of plastic-film mulch is now widespread in agriculture, particularly in cold, arid and semiarid regions of China. The mulch has numerous functions, including increasing the soil temperature, intensifying sunlight penetration , reducing soil evaporation and maintaining soil water content; also improving fertilizer-use efficiency, soil conservation, and reducing and eliminating weeds (1, 2, 3, 4). Over the past three decades, the amount of plastic film applied and area covered has increased dramatically from 6000 t in 1982, to 1.2 Mt in 2011, a 200-fold increase (Figure 1) (5). The area of crops with plastic-film mulching has continued to increase from only 0.12 Mha in 1982, to 4.9 Mha in 1991, 11.0 Mha in 2001 and 19.8 Mha in 2011(6).

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Figure 1. The amount of plastic-film mulch used in Chinese agriculture from 1982 to 2011.

Plastic-film mulch is widely applied, from the arid and semiarid regions in north China to the mountainous, cold regions in south China, such as the provinces of Inner Mongolia, Shandong, Henan and Hebei in north China, Xinjiang and Gansu in

northwest China, and Sichuan and Yunnan in southwest China. Shandong, Xinjiang and Sichuan are the leading provinces in the use of plastic-film mulch, using 148,100 t, 121,200 t and 71,000 t, respectively in 2008 (5).

scientific The plastic film utilization intensity index (kg/ha/yr), calculated by dividing the application quantity (kg) of plastic-film mulch by agriculture (ha covered) of the province or city, reflects the use of plastic-film mulch in the region. Xinjiang had the largest utilization intensity of plastic-film mulch with 34.8 kg/ha/yr in 2011 as a result of the special climate and agricultural activities in the region (5, 6). In Xinjiang, irrigation, especially drip irrigation under the plastic film, is widely utilized in agricultural production, resulting in a rapid increase in the quantity of plastic film used. Shanghai and Beijing also had high plastic-film utilization intensity for vegetable and fruit production in the peri-urban and urban areas. The provinces with significant agricultural production like Shandong, Hebei, Henan, Sichuan and Gansu, all had high (above 10 kg/ha/yr) use intensity indexes of plastic film. From 1991 to

Figure 2. Hillsides in rainfed areas covered with plastic-film mulch (Photo by Zhang Yajian, 2012)

2011, the intensity in all the provinces and cities had increased by 3 to 8 -fold (Table 1). Plastic-film mulch has been widely used in the production of grain, cotton, oilseeds, sugar, vegetables, melons, fruit and tobacco, to improve crop yields, save water, enable earlier harvesting, and reduce herbicide and pesticide use (4, 7). The crop with the largest use of plastic-film mulching is maize, especially in arid mountain

Table 1. The plastic-film utilization intensity index (kg/ha/yr) of Chinese provinces and cities.

region (Figure 2). In 2011,the area of plastic-film mulch for maize and vegetables was about 6.7 Mha, cotton, 3.4 Mha and peanut and tobacco, about 1.0 Mha.

2. Pollution by plastic-film residue The plastic films used in China are a macromolecule hydrocarbon compound made from polyethylene (PE) by adding antioxidants. They are of high molecular weight, highly stable and may persist in the soil under natural conditions. The plastic-film residue arising from largescale use is considered to be a risk factor for sustainable agriculture in China. Over the past three decades about 20 Mt of plastic film have been applied(5), and 2 Mt of plastic-film residue remain in the soil. The thin (48 Âľm) plastic film is extremely difficult to recycle because of the high labour requirement. Farmers have to harvest the film by hand or with machinery before sowing the subsequent crop (Figure3). In Xinjiang and Gansu, the large quantity of plastic-film residue remaining in the soil has affected agricultural activities and crop growth. The amount of residual plastic in the soil varies with the number of years of mulching, film thickness, sheet width, and the percentage of soil covered by the film in the treated area (the mulching ratio). Our results showed that Xinjiang had the maximum film input of 61 kg/ha and that Hebei had the minimum of 33 kg/ha. In Xinjiang, Gansu and Ningxia in northwestern China, the mulching ratio was high up to 80%, while in the southwest mountain areas and in northern China the mulching ratio was only about 40% (Table 2). According to the Ministry of Agriculture of China (5), the agricultural residual plastic-film in the 17 provinces averages 60 kg/ha over the 10-year period of application in the 1990s(8). The average plastic-film residue in farmland soils was 90 to 150 kg/ha, the severest pollution occurred

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Figure 3. Removing plastic-film residue in Gansu and Xinjiang (Photo by Yan Changrong, 2008).

in the cotton fields in Xinjiang with the average residue of 259 kg/ha (Table 2), and with the maximum plastic film residue of 381 kg/ha.

The plastic-film residue is considered to be a risk for sustainable agriculture as there are several adverse effects on the soil. The most important one is

Table 2. The use of plastic film and the residues of plastic in five representative regions

On average, the residual pieces of plastic film in the soil are 1-2500 cm2 in area, with most pieces being 4-25 cm2. The percentage of pieces >25 cm2 is 16% to 25%, the percentage of that from 4-25 cm2 is about 44%54%, while the pieces <4 cm2 accounts for 21%-40% of the total. Depending on agricultural activities and usage, the residue exists as flakes, curled pieces or cylindrical and spherical balls distributed horizontally, vertically or at any angle in the soil. 71.9% of the pieces are deposited in 0-0.1 m, 21% in the 0.1-0.2 m, 4.8% in the 0.2-0.3 m and 2.3% below 0.3m soil layer (Table 3) (Figure4). In general, The number of years use of plastic film was proportional to the depth at which residues were found(9, 10, 11, 12, 13). Soil depth

Chengan

Shihezi

that the residue can prevent the penetration and flow of water within the plough layer and surface layer of soil, reducing infiltration and affecting the water absorption of the soil (15, 16, 17, 18, 19, 20).

(DIBP), added to the plastic film during the production process is volatile, may diffuse into the mesophyll cells through the stomata of the plant, to damage the chlorophyll and limit its formation(2, 17), and thereby affect plant growth. When the quantity of plastic-film residue in the soil reached 37.5 kg/ha, the seedling numbers of winter wheat decreased by 25% and the tiller number decreased by 17%. Plastic-film residue may also limit the growth of the root systems of maize, eggplant, cabbage and peanut. Cotton yields were reduced by 4%, 8%, 12% and 19%, respectively when the amount of residual plastic in the soil was 80, 170, 280 and 370 kg/ha respectively (15, 16). Plastic-film residue not only affects the soil and growth and development of crops, resulting in a decrease in crop yield, but has other adverse effects. One is the death of cattle following ingestion of plastic film mixed with the stover used as cattle feed, while another is the aesthetic pollution from plastic-film residue deposited by roadsides, in ditches and along fences. It also binds around the wheels of a seeder or the teeth of a plough, and hinders the cultivation operations (Figure 5)(9, 10, 18).

3. Reducing plastic-film residue pollution 3.1 Use less plastic film

To save and reduce the input of plastic film in the field, a technique has been developed, which is called the

Figure 4. Plastic-film residue pollution in crop fields in Xinjiang (Photos by He Wenqing (Left, 2006) and Zheng Jiaming (Right, 2014).

The plasticizer, diisobutyl phthalate Tongchuan Zhengning

Mean

Table 3. The plastic-film residues in soil profile (depth, m) after 10-20 years used in four representative regions (%)

multipurpose plastic- film technique (Figure 6), that is, the use of plasticfilm mulch of medium thickness (15 Âľm), increased toughness, and high resistance to damage. After harvesting, it can be collected and reused for a subsequent crop or crops, which not only reduces the useof plastic film, but also saves time and labour and protects the environment.

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scientific

Figure 5. Some side effects of plastic residues pollution in China

In Gansu during 2013, the technique was shown to reduce the mulching ratio from 80%-100% to 50%-70% while maintaining a high crop yield (Table 4).

by machine. In China, the plastic film mulch for agricultural use is very thin with only half of thickness of that used in developed countries, fragile and easily damaged, and thus not easily reclaimed by the machines. Nevertheless, several kinds of reclaiming machines, such as roller and rake types are available and highly efficient in reclaiming plastic residues. We propose that a planter with a facility for reclaiming plastic residue from the previous crop is the key to future development (23, 24, 25).

3.3 Mechanization of residual plastic recycling technology

In developed countries, plastic film is generally used in vegetable, fruit and other cash crops.

4. Conclusions Table 4. The economic analysis of Multipurpose plastic-film mulch technique for crops in Gansu 3.2 Use of degradable plastic film

Photodegradable and biodegradable plastic to replace PE plastic film (21) would have the advantage of reducing residue pollution (22). Cost of degradable plastic film is the main obstacle to its use in China. An economic assessment of biodegradable and PE plastic film for cotton production showed that the price of biodegradable film was double, although the total input costs of biodegradable film with different thicknesses increased by only 12%, 41% and 69%, respectively, because of exclusion of the cost of collecting biodegradable residues (14) (Table 5). Considering the environmental effect, biodegradable film has a great potential for agricultural application in the future.

In these countries, the plastic film has 15 Âľm thickness, and is easy to reclaim Items

The continuous use of thin stable PE plastic-film mulch for improving crop production in cold and dry regions of China has led to large quantities of plastic residue building up in the soil. It

PE plastic film

Biodegradable plastic film

Thickness (Âľm) Colour

Transparent

Price (RMB yuan/kg) Amount of plastic film (kg/ha) Cost of plastic film (RMB yuan/ha) RMB yuan/ha Total costs (RMB yuan/ha) Percentage cost increase (%)

Table 5. Annual economic assessment of biodegradable and PE plastic film in cotton production

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scientific It has begun to reduce crop growth and yields, particularly in cotton which has the longest term use among crops. For sustainable agriculture, the continuous use of plastic-film mulch needs to be reduced in the future. The degradable plastic, thicker and stronger plastic film for multiple-year use, a reduction in the mulching ratio and the use of cultivators/seeding equipment that can pick up plastic residue are recommended for reducing plastic pollution. These techniques need to be explored.

Acknowledgement We thank two reviewers and Dr. David Frape for their valuable suggestions and comments, which led to substantial improvements of this paper. This study was partially supported by the Chinese National Scientific Foundation (No. 31370522), the 12th five-year plan of National Key Technologies R&D Program (No. 2012BAD09B01) and “948” project from Ministry of Agriculture (2014-Z6). Dr. He Wenqing is corresponding author.

References 1. Li Fengmin, Wang Jun, Xu Jinzhang, Xu Huilian (2004) Productivity and soil response to plastic film mulching durations for spring wheat on entisols in the semiarid Loess Plateau of China. Soil and Tillage Research 78, 9-20. 2. Yan Changrong, He Wenqing, Mei Xurong (2010)Agricultural application of plastic film and its residue pollution prevention . Beijing: Science Press. pp. 76~86. 3. Wang Hanbo, Gong Daozhi, Mei Xurong, Hao Weiping (2012) Dynamics comparison of rain-fed spring maize growth and evapotranspiration in

Chinese agricultural farm worker

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plastic mulching and un- mulching fields. Transactions of the Chinese Society of Agricultural Engineering 28 (22), 88-94. 4. Gan Yantai, Siddique K H M, Turner N C, Li XG, Niu J-Y, Yang C, Liu L, Chai Q (2013) Ridgefurrow mulching systems - an innovative approach for boosting crop productivity in semiarid rain-fed environments. Advances in Agronomy 118, 429476. 5. Ministry of Agriculture P. R. China. China agricultural statistics yearbook, Beijing: Chinese Agricultural Press. 6. Rural Society Investigation Department of National Statistical Bureau. China Rural Statistics Yearbook. Beijing: China Statistics Press, 2002, 2012. 7. Scarascia-Mugnozza G, Sica C, Russo G (2011) Plastic materials in European agriculture: Actual use and perspectives. Journal of Agricultural Engineering 42 (3), 15-28. 8. Wang Xiaofang, Shen Maoxiang (1998) Farmland plastic film-Hope and dawn of Chinese agricultural development. Countryside Science and Technology Department of Science of China. 9. Yan Changrong, Mei Xurong, He Wenqing, Zheng Shenhua ( 2006 ) Present situation of residue pollution of mulching plastic film and controlling measures. Transactions of the Chinese Society of Agricultural Engineering 22 (11), 269272. 10. Yan Changrong, Wang Xujian, He Wenqing, Ma Hui, Cao Silin, Zhu G (2008) Study on the residue of plastic film in cotton field in Shihezi, Xinjiang. Acta Ecologica Sinica 28, 3470-3484. 11. Ma Hui, Mei Xurong, Yan Changrong, He Wenqing , Li Kang ( 2008 ) The residue of mulching plastic film of cotton field in North China. Journal of Agro-Environment Science 23, 570-573. 12. He Wenqing, Yan Changrong, Zhao Caixia, Chang Ruifu, Liu Qin, Liu Shuang (2009) Study on the pollution by plastic mulch film and its countermeasures in China. Journal of AgroEnvironment Science 28, 533-538. 13. He Wenqing, Yan Changrong, Liu Shuang, Chang Ruifu, Wan X, Cao Silin, Liu Qin (2009) The use of plastic mulch film in typical cotton planting regions and the associated environmental pollution. Journal of Agro-Environment Science 28, 1618-1622. 14. Zhao Caixia, He Wenqing, Liu Shuang, Yan Changrong , Cao Silin (2011) Degradation of

biodegradable plastic mulch film and its effect on the yield of cotton in Xinjiang region, China. Journal of Agro-Environment Science 30, 1616-1621. 15. Zhao Surong, Zhang Shurong, Xu Xia, Xu Lichao, Zhang Donghe, Zhang Xinmin , Wang Jinfeng, Xu Ligong , Qi Ying ( 1998 ) Study on the agricultural plastic sheeting residue pollution. Agro-environment and Development 3, 7-10. 16. Cheng Guihua, Liu Xiaoyang, Liu Yuanjun, Jin Weixu, Mu Luming, Yan Zhonghui (1991) Study on permissible value of plastic residual piece in field soil. Soil and Fertilizer 5, 27-30. 17. Nan Dianjie, Xie Honge, Gao Liangsheng, Zhang Dongmei , Zhao Haizhen, Ren Pinghe , Chai Shiwei (1996) Study of the influence of the residue film on soil and cotton growth in the cotton fields. Acta Gossypii Sinica (now Cotton Science) 8 (1), 50-54. 18. Gao Qinghai, Lu Xiaomin, (2011) Effects of plastic film residue on morphology and physiological characteristics of tomato seedlings. Journal of Tropical and Subtropical Botany 19, 425429. 19. Chang Ruifu, Yan Changrong (2012) Research report on overall current situation on agricultural plastics residuals pollution and its countermeasures. Beijing: China Agricultural Science and Technology Press, pp. 13-15, 41. 20. Lu Shengzeng, Zhou Zhenfeng, Yan xishi (2013) Environmental problems and control ways of plastic film in agricultural production. Applied Mechanics and Materials 295, 2187-2190. 21. Ammala A, Bateman S, Dean K, Petinakis E, Sangwan P, Wong S, Leong KH (2011). An overview of degradable and biodegradable polyolefins. Progress in Polymer Science, 36(8), 1015-1049. 22. Kyrikou I, Briassoulis D (2007) Biodegradation of agricultural plastic films: a critical review. Journal of Polymers and the Environment, 15(2), 125-150. 23. Cao Silin, Wang Xujian (2008) The research status of plastic film residual pollution control and the patent strategy. Agricultural Machinery 20, 7778. 24. Cao Silin, Wang Xujian, Shen Congju, Lu Bing (2000) Patent analysis on mechanization technology of retrieving the used plastic film. Chinese Agricultural Mechanization 4, 48-50. 25. Cao Silin, Wang Xujian, Wang Min, He Yichuan, Liu Yun (2012) Design and experimental research on 1LZ series combined tillage machine. Acta Agriculturae Boreali- Occidentalis Sinica. 21,

scientific

Aquaculture: are the criticisms justified? II â&#x20AC;&#x201C; Aquacultureâ&#x20AC;&#x2122;s environmental impact and use of resources, with special reference to farming Atlantic salmon Dr C J Shepherd BVSc, MSc, PhD, MRCVS and Professor D C Little BSc, MSc, PhD, FSB* Address for correspondence: Prof D C Little,* Institute of Aquaculture, University of Stirling FK9 4LA, UK. Email: dcl1@stir.ac.uk Summary Salmon farming is the most highly developed form of large scale intensive aquaculture owing to its productivity growth and technological change. The fundamental questions are how farmed salmon compares to other food production systems and prospects for its improved sustainability. This paper reviews the criticisms of Atlantic salmon farming, in particular those relating to its ecological and environmental record. Compared with terrestrial livestock, fish are better suited for farming, being cold-blooded (ectothermic) with neutral buoyancy in water, which enhances production efficiency, and farmed fish are more productive than wild fish as they use less energy and lack predators. Some of the criticisms of salmon farming are entirely erroneous (e.g. that hormones or growth promoters are used). Others are unfounded today due to the rapid advances made since the industry started in the 1970s (e.g. that antibiotics are overused; that health risks exist from eating salmon due to the presence of contaminants; that using fishmeal and fish oil is unsustainable and threatens wild fisheries; that salmon farm effluent threatens the coastal ecosystem). It is concededthat infestation of salmon (Lepeophtheirus salmonis) by sealice and the risk of salmon escaping from farms remain valid concerns. Sealice numbers can readily build up in salmon farms and, even if satisfactorily controlled in the cages, infectious stages of the parasite may leave the cage and potentially infect adjacent wild salmon populations. Escaping farmed salmon may contribute to this, but can also potentially breed with wild salmon and affect the native salmon gene pool. However, there is no convincing evidence that the salmon farming industry is responsible for the widespread decline in wild salmon and sea trout populations, which began to decline before salmon farming was established. Life cycle analysis suggests salmon farming and cod fishing are comparable. However, catching cod prey species (e.g. capelin) to use as salmon feed ingredients is a far more efficient way of supplying nutrients for human consumption than leaving such prey in the sea and harvesting the resulting cod. Recent detailed studies of the salmon farming industry in Norway have shown that it is a more efficient way of producing nutrients for human consumption than either pig or chicken farming, as demonstrated by its climate impact, area of land occupation, and use of non-renewable phosporus resources. Farmed salmon retain nutrients more efficiently and are better converters of feed nutrients to nutrients for human consumption than the most efficient land animal production. There is no evidence that the progressive replacement of marine protein and oil by plant protein and oil is more sustainable than salmon farming based on wild-caught fish (or their by-products). At the same time it causes the farmed salmon content of long-chain polyunsaturated fatty acids (PUFAs) (especially Eicosapentaenoic acid or EPA and Docosahexaenoic acid or DHA) to fall with negative implications for consumers (pending availability and consumer acceptance of cost-effective alternative PUFAs), unless they compensate by consuming more oil-rich fish or take PUFA supplements. The salmon farming industry continues to innovate and prioritise to improve its sustainability, to improve seawater survival and to find cost-effective alternatives to the limited supply of fish oil, which is currently the only practical source of EPA and DHA. A subsequent paper will consider the extent to which the improved environmental track record and resource efficiency of Atlantic salmon farming is duplicated by other aquaculture species. Although it has been shown that much of the criticism of salmon farming is false or exaggerated, the industry is small in a global aquaculture context. Do these (or other criticisms) hold true, for example, with the farming of warmwater shrimp or carp? Such questions are relevant when considering aquacultureâ&#x20AC;&#x2122;s global role in food security and how best to guide its sustainable development. Keywords aquaculture; eco-efficiency; environmental impact; life cycle analysis; productivity; salmon farming; supply chain; sustainability.

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scientific Abbreviations

FAO Food and Agriculture Organisation; FCR Food conversion rate; FIFO Fish-in, Fish-out ratio; GM Genetic modification; PCB Polychlorinated Biphenyls; PPR Primary Productivity Requirement; EPA Eicosapentaenoic acid; DHA Docosahexaenoic acid; DNA Deoxyribonucleic Acid; PUFA Polyunsaturated Fatty Acid; HACCP Hazard Analysis Critical Control Point; EFSA European Food Safety Authority; HCH Hexachlorocyclohexane; LCA Life Cycle Analysis.

Glossary A coproduct is a product produced jointly with another product; an epizootic is a disease that appears as new cases in animals at a substantially elevated incidence rate and is an analogous term to ‘epidemic’ applied to human populations; eutrophication is the ecosystem response to the addition of artificial or natural substances (e.g. nitrates and phosphates through fertilizers or sewage) to an aquatic system; To fallow an aquaculture site means leaving it empty of fish for a period without restocking in order to allow the seabed to return to normal condition and to restore the site’s productivity; feed conversion rate = (kg feed fed)/(kg bodyweight gain); fish-in fish-out ratio (when used about aquaculture) refers to the input of fish materials (usually fishmeal and fish oil) as feed ingredients compared to the resulting output of farmed fish; fishmeal trap is a term denoting the

concern that increased demand for feed by aquaculture will increase fishing pressure on wild stocks and hence threaten the sustainability of the associated capture fisheries; a gadoid is a soft-finned marine fish which is a member of the family Gadidae including cod; a genome is the complete set of DNA within a single cell of an organism and genomics is the genetic discipline that sequences, assembles, and analyzes the function and structure of genomes; genetic modification (GM) (e.g. of a fish or a plant) results in a genetically modified organism (GMO), which possesses a novel combination of genetic material obtained through the use of modern biotechnology; life cycle analysis (LCA) is a technique to assess environmental impacts associated with all the stages of a product's life from start to finish; an oil adjuvant is an immunological vehicle for enhancing the potency of a vaccine, eg by emulsification in mineral oil;

Figure 1. Global production of farmed Atlantic salmon 2000-2013 (tonnes x 1000) Source: Kontali Analyse (2013)

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Organoleptic properties are the aspects of food or other substances as experienced by the senses, including taste, sight, smell, and touch; a poikilotherm is an organism with an internal temperature which varies, usually in response to changing environmental temperature and is sometimes known as an ‘ectotherm’ or ‘cold-blooded’; a reduction fishery is a fishery that ‘reduces’ its catch to fishmeal and fish oil and is also known as a ‘feed’ fishery or a ‘forage’ fishery; salmonids are fish which are members of the Salmonidae, or salmon and trout family, which belong to the order Salmoniformes; a smolt is a juvenile salmon in freshwater or estuarine conditions which has become silvery in colour and is ready to go to sea; triploid fish have three sets of chromosomes instead of the normal two (‘diploid’), usually because the egg is physically shocked shortly after fertilisation occurs, resulting in sterile fish.

scientific 1. Introduction

quaculture is a more varied activity than land animal farming, encompassing a range of systems for rearing finfish, molluscs, crustaceans, and aquatic plants, in freshwater or seawater. From 1980 to 2010 world food fish production by aquaculture has expanded almost 12-fold at an average annual rate of 8.8%, although slowing to an average annual rate of only 6.3% over the last decade to reach 63.6 million tonnes in 2011 (excluding aquatic plants).1 The contribution of global aquaculture to world seafood production for human consumption has risen from 9% in 1980 to 47% in 2010. The hunting of fish and the problem of static or declining fish stocks represent an uncertain and erratic way to meet demand consistently on a long-term basis. The high price and seasonal supply of wild salmon helped to encourage pioneering investment in farming of Atlantic salmon (Salmo salar) in the late 1960s and the industry took off in Norway and the UK in the 1980s,

followed by North America and then Chile, as retailers and food service companies found they were able to place contracts for year-round supply of consistent product. The development of salmon farming has been characterised by progressive industrialisation and commoditisation. However, aquaculture, especially the farming of carnivorous fish like salmon, has attracted intense and often misinformed criticism. This has been linked mainly to the use of diets containing fishmeal and fish oil or minced wet fish, â&#x20AC;&#x201C; the subject of a previous paper2 in World Agriculture. At the same time improvements in diet formulation and feeding systems have resulted in feed conversion rates (FCR) improving from almost 3.0 in 1980 to just over 1.17 in 2012,3,4 meaning that the quantity of feed needed per unit liveweight gain has reduced by approximately 60% over the period. Global production of farmed Atlantic salmon reached 2.0 million t (whole round, bled weight) in 20125 which is small (ca. 3%) in relation to estimated total global aquaculture production.1 Fig. 1 shows global production of Atlantic salmon has increased from

2002 to 2013 (estimated) by main production regions, whereas Fig. 2 shows a stagnating wild fish catch compared with aquaculture supply since 2000, with a forecast to 2020. Atlantic salmon farming is recognised as the most highly developed form of intensive fish cultivation. Accurate information is also available enabling detailed analysis of its efficiency, especially for the Norwegian salmon farming industry, which dominates global salmon production and is the technical model for intensive cage-based aquaculture. This paper surveys the main criticisms of aquaculture, with special reference to Atlantic salmon. When assessing the validity of such criticisms, the fundamental question with respect to salmon aquaculture is how farmed salmon compares to other food items and production systems and if developments in the salmon industry will lead to improved sustainability. The answers to such questions have implications for other forms of aquaculture and may help assess the potential role for global aquaculture in future food production and food security.6,7

Total capture Total aquaculture Total world

Figure 2. Global fishery and aquaculture production, 2000-2011 (tonnes x million) Source: FAO Fisheries and Aquaculture Statistics and Information Branch 2013. Capture production 1950-2011. Aquaculture production 1950-2011. Available at http://www.fao.org/fishery/statistics/en

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scientific 2. Suitability of fish for farming

3. Salmon productivity growth and technological change Fig 3 shows the development of Norwegian farmed salmon production over the period from 1985 to 2011, the average cost of production and the average export price. Production has increased from 31 177 to 1 005 600 t while the production costs and sales prices have fallen steeply. Thus in 1986 the average production cost was 76.1 NOK/kg but it had fallen to 15.5 NOK/kg in 2005 (1 NOK or Norwegian krone equals 0.16 US dollar as of Dec. 2013), since when costs have slightly risen and prices have fluctuated but the industry has remained profitable. The price reduction has enabled the industry to continue expanding into new markets. This could not have taken place without lower costs due to increased productivity and technological change.10 This is because farmers have become more efficient (i.e. growing larger salmon more quickly with fewer losses) while at the same time they have benefited from improved inputs (including improved stock, better feed and rearing systems) and have gained economies of scale

from establishing larger farms. Thus improvements in diet and feeding systems, as well as better fish health, have improved FCRs for Norwegian salmon from almost 3.0 kg feed/kg salmon body weight gain in 1980 to just over 1.17 kg/kg in 2012. This is partly due to a marked change in the ratio of protein to oil used in feeds related to the development of vacuum coating of lipids. Crude protein levels of 45% and fat of 18% in the 1980s have changed to 36% and 38% respectively in the 2000s.11The salmon farming industry has been criticised for its supposed reliance on dietary marine ingredients. However, the quantity of wild fish used to produce the fish meal and oil needed to rear 1 kg of farmed salmon (i.e. the Fish-in, Fish-out ratio or FIFO) has decreased from 4.4 and 7.2 in 1990 to 1.4 and 2.3 respectively in 2010; when corrected to take account of the use of processing by-products of capture fishing, the values in 2010 were 1.1 and 1.8 respectively.12 The limited and fluctuating supply and cost of marine ingredients have encouraged the Norwegian salmon farming industry progressively to substitute plant ingredients for marine ingredients, and there has been a further change since 2010, so current FIFO ratios are probably below 1.0 for fishmeal and close to 1.0 for fish oil. These developments have progressively challenged the criticism that aquaculture of ‘carnivorous species’ (e.g. salmonids) is unsustainable (see 4(i) below).

1,000 tonnes

Compared with warm-blooded animals, cold-blooded ‘poikilotherms,’ such as fish, are more efficient converters of feed energy to bodyweight, especially under farming conditions. Firstly they have lower maintenance and respiratory costs.8 Their protein metabolism uses less energy since they excrete ammonia directly into the environment instead of excreting urea or uric acid. Also their neutral buoyancy in water saves energy by avoiding the need for a heavy skeleton to counteract gravity. In general this means a greater proportion of the fish carcase is edible compared with land animals; this is especially the case for carnivorous fish which have a shorter digestive tract compared with fish species more adapted for a vegetarian diet. Compared with fish in natural environments, farmed fish show improved growth and nutrient retention because they are protected from predators and utilise less energy in accessing food.9 Compared with intensively housed land animals, it is difficult to maintain a controlled environment within a fish farm and maintain biosecurity. This is especially the case in seawater cages and will be considered further, together with the prospects for mitigation. Most aquatic animals have far greater reproductive capacity than terrestrial livestock, but also allocate less resource to reproduction. Although many fish have microscopic larval

stages, the cost of producing salmon fry is low as they produce relatively large eggs (with attached yolk sacs), which in turn develop into larvae capable of feeding readily on inert hatchery diets once the yolk sac contents are fully consumed.

Figure 3. Norwegian farmed salmon volumes (tonnes x 1,000) compared with production cost and export price (Norwegian Krone) in real terms (2011=1), 1985-2011 Source: Norwegian Directorate of Fisheries: Norwegian Seafood Export Council

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scientific 4. The criticisms related to ecological impact and environmental pollution (i) Introduction

(ii) Effluent discharge/Organic waste

Organic waste beneath salmon farms comprises fish faeces and unconsumed feed, which can accumulate on the seabed. This may impact on local seabed fauna and increase the risk of eutrophication with consequent negative effects on productivity.10 During the 1980s many salmon farms were located in sheltered sites close to shore to reduce potential storm damage. As a consequence, so called ‘dead areas’ developed on the seabed under the cages. Since then salmon farming systems have evolved to use more exposed locations with stronger currents and deeper water beneath more robust cage groups (which are regularly rotated between farm sites to enable fallowing), ensuring waste materials are flushed to sea and salmon have optimal water quality. Additionally improvements in FCR have reduced the feed requirement per tonne of salmon produced by around 60% since the 1980s. The regulatory framework has also become more sophisticated, e.g. in Scotland

Antibiotic (kg)

Any production process interacting with the natural environment can potentially compromise the environment. For instance it has been claimed that the use of dietary marine ingredients in fish farming causes unsustainable damage to wild fish stocks being harvested for fishmeal and fish oil, and that reduction fisheries will therefore inevitably become overfished.13 This so-called ‘fishmeal trap’ has not occurred, however, due to dietary innovation, increased use of fish process trimmings, and to the increasingly responsible management of reduction fisheries.10,14 Therefore the criticism is no longer valid except in the case of ‘trash fish’ feeding in South East Asia.2 However, there is a range of local environmental issues which is claimed to have detrimental effects on the local and regional environment. Salmon is normally farmed in floating cages, hence by definition takes place in ‘open’ systems in which water exchange occurs continuously with the wider environment and economic performance of the fish in such

systems demands that water quality remains at an optimum. The implications for salmon farming are considered below, together with the allied risks of disease transmission to the wild, farmed salmon escapement, contamination from treatment chemicals, and effluent discharge/organic waste.

regulation of benthic impact is exercised through rigorously applied discharge controls, the use of particle tracking models, which predict the seabed footprint, and the ‘steady state’ and ‘limiting factor’ principles.15 A recent detailed NOAA report concludes that marine cage culture has ‘minimal’ impacts to the environment where farms are appropriately sited and properly managed.16 (iii) Antibiotics, chemicals, and hormones, etc.

Although the use of antimicrobial growth promoters is widespread in intensive production of poultry and pigs, it should be noted that they are not used in salmon farming at all. Nor are hormones used in salmon farming despite frequent media comments suggesting otherwise. Fig 4 illustrates the rise and fall of antibiotic use in Norwegian salmon farming over the period 1980 – 2011. It can be seen that, after reaching a peak in the 1980s, use of antibiotics fell quickly to very low levels despite a rapid and continuing increase in salmon production. This was almost entirely due to the successful introduction of oil-adjuvantedvaccines in controlling bacterial diseases. Antibiotics are only allowed on veterinary prescription and the amount used per kilo of meat from terrestrial livestock in Norway is 20 times the amount used for farmed salmon.7

Salmon production (tonnes x 1000)

For increasing use of plant ingredients and other challenges, see section 8(viii).

Figure 4. Annual use of antibiotics (kg) in Norwegian salmon production, 1980-2011 Source: Norwegian Directorate of Fisheries

WORLD AGRICULTURE 41

scientific There has been a similar reduction in the use of medicines to control sealice (Lepeophtheirus salmonis) infestation (e.g. azamethiphos; cypermethrin), and in the use of antifoulants to reduce build-up of algae on cages (e.g. using copper-based paints). In the case of sealice, an integrated pest management approach has increasingly become the norm, resulting in much diminished severity of infection in recent years despite the declining effectiveness of individual drugs. Treatment of affected fish has been by means of either in-feed antiparasitic drugs (emamectin benzoate; teflubenzuron) or by adding medicinal products applied as baths (e.g. peroxide) to the water in the cage. Treatment of affected fish by means of in-feed or bath treatments in some instances is only partially successful due to the emergence of resistance. There is also increasing use of biological control by the introduction to salmon cages of wrasse of various species (e.g. Labrus bergylta) or lumpsucker fish (e.g. Cyclopterus spp.), which feed directly on the lice attached to salmon skin; this approach has obvious environmental attractions and is now stimulating an interest in cultivation of these so-called ‘cleaner’ fish to supply to the salmon farming industry. A key issue is the cost-effective production of disease-free juvenile cleaner fish and their management in commercial systems based on fish being stocked and harvested on ‘all-in, all-out’ principles. Use of antibiotics can never be eliminated entirely for reasons of animal welfare and the possibility of emerging bacterial diseases. However, there are continuing problems in controlling sealice infestation and it is estimated that during 2012 around 45% of Norwegian salmon farming sites were treated for sealice, with each being treated on average 2.5 times over the production cycle. There is increased recognition of the importance of husbandry measures, such as zonal management among neighbouring salmon farm units (taking account of industry codes of good practice), and selective breeding for increased resistance. The more recently established Chilean salmon farming industry continues to struggle with disease problems and lags behind the effective control achieved in Norway, Scotland and North America without large scale use of medicinal products.

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Freshwater production of salmon smolts – note use of underwater lights for photoperiod control of smoltification (Courtesy of Marine Harvest Ltd., Scotland) (iv) Transmission of disease agents to and from wild stocks

The early growth of salmon farming was severely challenged by epizootics of infectious disease, in particular bacterial septicaemias, such as furunculosis (due to Aeromonas spp.) and vibriosis (due to Vibrio spp.). Routine vaccination of smolts by injection prior to seawater transfer was found to be highly effective. An exception is Salmon Rickettsial Syndrome in Chile due to Piscirickettsia salmonis for which a satisfactory control method is so far lacking, although vaccines are under trial. An increasing range of viral diseases has been found to affect farmed salmon and can cause severe losses, although viral vaccines against Infectious Pancreatic Necrosis and Pancreas Disease are now in routine use. The sources of such infections are not always clear but there is increasing evidence that most if not all the causative organisms have been present in wild fish populations since before the start of salmon farming. The presumption is that they rarely cause disease in wild populations, but can be transmitted to adjacent farmed stocks in hatcheries or cage farms where clinical disease can spread quickly in unprotected salmon under conditions of high stocking density. Whereas bacterial and viral disease epizootics in farmed salmon may cause shedding of pathogens into the environment, there is little evidence that this causes clinical disease in adjacent wild fish, apart from occasional mortalities seen in wild gadoid fish, e.g. saithe (Pollachius

virens), which have gained access to the salmon cage. However, parasitic infestations of wild Baltic strains of Atlantic salmon with the skin fluke Gyrodactylus salaris caused severe losses in susceptible Atlantic salmon populations when infected fish were transplanted to Norway and released into the wild. In the same way there is concern that sealice infestation in farmed salmon (in Europe due mainly to L. salmonis and in Chile due mainly to Caligus rogercresseyi) potentially threatens wild salmon populations. Sealice occur naturally in the wild and, long before salmon farming started, sealice epizootics caused mortalities of wild Atlantic salmon in Canada17 while the presence of a few sealice on wild salmon has traditionally been accepted as a positive indication of freshly searun fish. However, under farming conditions these crustacean skin parasites can multiply rapidly and infectious stages swim actively to find a suitable host elsewhere within the cage, or potentially leave the cage and may infest migrating wild salmon in the vicinity. For this reason, treatment aims to prevent the development of sexually mature breeding lice, in order to reduce infection pressure for both farmed and wild salmonid populations, rather than just for farmed fish welfare. Salmon farming does not appear to prejudice wild salmon populations with the possible exception of the effects of sealice. However, new problems will emerge and continuing vigilance is needed to control fish movements and hence limit the spread of fish disease organisms.

Individual escapees x 1000

Salmon production (tonnes x 1000)

scientific

Figure 5. Number of escaped salmon in relation to Norwegian salmon production, 1993-2012 Source: Norwegian Directorate of Fisheries (v) The effect of salmon farming on wild stocks

The number of Norwegian farmed salmon reported as escaping each year is relatively low and fairly stable (Fig. 5) when compared with the increasing production, although it remains a continuing problem. Escaped fish are likely to compete with wild salmon and may breed with them, hence affecting the gene pool (so-called â&#x20AC;&#x2DC;genetic pollutionâ&#x20AC;&#x2122;). Although the outcome of escapee-wild fish interactions varies with environmental and genetic factors, modelling suggests they may be negative for wild salmon18 and that gene flow from escaped farm fish to native wild fish may lead to genetic and behavioural changes in wild populations in the direction of domesticated salmon. It is also possible that wild populations may suffer depressed productivity caused by ecological interactions with escaped farm salmon and their offspring.19 At the same time a concern is that escaping farmed salmon could transmit disease organisms to wild populations, especially sealice (see 4(iv) above). Compulsory tagging of smolts prior to their being stocked in salmon cages is being considered by the Norwegian authorities for greater traceability of farmed salmon should they subsequently escape, in order to aid policing and the ability to penalise offending farms. Other than adopting genetically modified (GM) technology

(should approval be granted), the use of triploid salmon is the only way to rear sterile salmon in order to avoid any risk of genetic pollution from escaped fish (see 8(iv)), whereas the cost of on-shore tank production is likely to remain prohibitive in most cases. Notwithstanding the above concerns, there is little scientific evidence to support the claim that salmon farming has caused the widespread decline in wild salmon fisheries in Europe and North America. Mismanaged capture fisheries, habitat destruction, and excessive mortality from fishing have resulted in wide-scale extirpations, depletions and loss of biodiversity in both Atlantic and Pacific salmon (Oncorhynchus spp.); this occurred long before commercial salmon farming started in the 1970s.20,21 For Norway there seems to be no measurable impact at the national level of salmon farming on the wild salmon stocks in Norwegian rivers7. In Scotland anglers continue to blame salmon farming for the collapse of the west coast populations of Atlantic salmon and sea trout (Salmo trutta) in the 1980s. Thus sea trout anglers blame salmon farming for the demise of the Loch Maree sea trout fishery22 and claim that by 1980 the fishery was in decline, although the scientific evidence for this stock status in 1980 is not clear cut.23 There seems no doubt that the fishery was collapsing in the late 1980s by which time salmon farming was established in

the area. It therefore remains a possibility that the effect of neighbouring salmon farms (e.g. due to sealice) exacerbated the decline of a fishery that was already under stress due to environmental factors, such as the effect of freshwater acidification. A more likely explanation for this timetable of events at Loch Maree22 is the introduction of legislation in 1984 (Inshore Fisheries Act), which opened up the zero to 3 mile coastal area to all mobile fishing gear. The fact that farmed salmon has brought down the price and largely replaced wild capture salmon in the market, is probably contributing to the rebound of some salmon stocks for both Atlantic and Pacific salmon.6 (vi) Contaminants from marine feed ingredients entering the food chain

The use of fishmeal and fish oil will tend to concentrate contaminants present at low levels in forage fish and hence result in potentially elevated levels in farmed fish. This has raised concern about the human health risks from consumption of farmed salmon and particular prominence was given to a report24 highlighting the presence of low levels of dioxins and PCBs in farmed salmon. However, subsequent studies have shown the risks were greatly exaggerated (if they existed at all) and that any possible risks are in any event greatly outweighed by the resulting health benefits.25

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scientific More recent data showed that farmed salmon and trout contained on average lower levels of dioxins and PCBs than wild caught salmon and trout, at least for Europe.26 This may reflect the requirement since 2005/2006 for fishmeal and fish oil in the EU to be routinely tested for contaminants prior to manufacture.27 It is of interest that fish oil manufactured within the EU from forage fish caught in the Baltic is normally above the required maximum levels for certain contaminants and can only be sold after further purification steps under EU control; whereas wild-caught Baltic salmon may be legally offered for sale without any such control. The permitted maximum levels of contaminants set by the EU for those contaminants perceived as undesirable in feeds and foodstuffs are laid out in Directive 2002/32/EC (undesirable substances in animal feed) and in Regulation EC No 466/2001 (maximum levels for certain contaminants in foodstuffs); these regulations cover dioxins, PCBs and heavy metals (e.g. mercury, cadmium, lead, arsenic), as well as pesticides (e.g. toxaphene, HCH isomers, endrin, endosulfan, aldrin and dieldrin). In any event it seems clear that the progressive reduction in levels of dietary marine ingredients due to substitution by vegetable ingredients has also served to reduce the content of certain contaminants in raw marine feed materials, and hence trace levels of any such substances that may be present in the salmon product.

5. Comparison with conventional fishing In 2011 global capture fish volume was 93.5 million tonnes of which 67.2 million tonnes was of food fish, as compared with 63.6 million tonnes of

world aquaculture production of food fish.28 It seems probable that by 2015, or earlier, world food fish production for human consumption by aquaculture will for the first time exceed food fish production for human consumption from capture fisheries.29 Capture fishing shows an overall global pattern of static or declining catch with increasing marginal costs. The problems of overfishing, by-catch, discards and habitat destruction are well known. The World Bank estimated that global fisheries currently run a net economic loss of about US$5 billion per year30 and they take in as much as US$32 billion per year in subsidies;31 the resulting artificial inflation of profits encourages increased effort regardless of the condition of the fishery and discourages conservation.32 In addition to the use of fish process trimmings, the marine ingredients used in salmon diets rely on capture of small pelagic species usually occurring in tight shoals which are caught using purse seines without impacting the seabed and with very low by-catch levels. Also it is recognised that most of the assessed forage fisheries operate within the limits that would be considered consistent with current good industry practice in the context of single species management regimes.14 Comparisons of aquaculture with capture fishing are not straightforward as the energy transfer between different trophic levels is not well documented, but farmed fish are inherently more efficient due to their being protected from predators and not needing to forage for food (section 2). Accepted theories on energy and matter flow between trophic levels indicate that farmed salmon (and carnivorous marine finfish culture generally) appropriate less ocean primary production than commercial

capture fishing.33 Assuming a 10% energy flow between trophic levels, producing 1 unit of predatory fish (such as wild salmon) requires 10 units of food (largely small pelagic fish), or more if by-catch values are taken into account.34 Even when compared with the 2 â&#x20AC;&#x201C; 5 units of pelagic fish formerly needed to produce one unit of farmed fish,35 there was a clear ecological advantage in favour of farmed salmon. Today, the comparison is even more in favour of farming due to the dominance of plant ingredients in salmon feed. The evidence clearly indicates that aquaculture can be a more efficient use of living marine resources than commercial fishing33 if sustainably produced marine ingredients are used. This has been well documented in the case of farmed Norwegian salmon as compared with capture fishing of wild cod (Gadus morhua). It was shown that harvesting fish higher in the marine food chain, such as cod, is far less efficient in providing marine nutrients for human consumption compared to harvesting capelin (Mallotus villosus) to manufacture fishmeal and oil used in salmon production. Capelin is an important food source for cod, but using the capelin resource to produce salmon gave nearly 10 times more marine protein, 15 times more energy and 6 times more EPA and DHA for human consumption (including the cod liver oil), when compared with harvesting the cod resource.12 Whereas farmed salmon and wildcaught cod are comparable when subjected to life cycle analysis (LCA) in order to compare their environmental impacts, it is of interest that the nutritional output of marine protein and essential fatty acids for human consumption from these two alternative ways of using the capelin resource is very different.36,37

Close up view of salmon farm in Western Isles â&#x20AC;&#x201C; note use of circular plastic pens with overhead anti-predator nets and central supports (Courtesy of Marine Harvest Ltd, Scotland)

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scientific

Figure 6. Global production for 2011 of beef, pork, chicken and fish (capture fish versus aquaculture) Note: Land animal meat as carcass weight (millions of tonnes): capture fish and aquaculture as live weight equivalent (millions of tonnes) Source: FAOSTAT

6. Comparing salmon farming with land animal farming Estimated 2011 global production of beef, pork, chicken, and fish (capture fisheries and aquaculture) is given in Fig. 6 (note FAO production data for land animal meat and for fish are not readily comparable being expressed in two different product forms: meat in carcass weight and aquaculture/ capture in live weight equivalent; FAOSTAT data38 on production of land animals is given in tonnes as carcass weight, but there is no comparable figure for live weight equivalent). It is likely that by 2012 annual global aquaculture production will have exceeded global beef production. Table 1 compares harvest yield, edible yield, energy retention, protein retention and energy retention in the edible parts of Atlantic salmon, pig, chicken, and lamb, as well as FCR.39 It can be seen that the processing yield of Atlantic salmon is high compared with domesticated land animals, reflecting a relatively low skeletal weight.40 Comparing the amount of protein in edible parts to the amount of protein fed to the animal, salmon retain the most protein (31%) relative to pig, chicken and lamb; salmon also retain the most energy (23%) in the edible parts39. The FCR data show that the most efficient converter is farmed salmon compared with land animals. Although not included in the table, among the least efficient is wild salmon with an FCR of ca.10.4 The willingness of the Norwegian salmon industry to divulge accurate and comprehensive data has enabled rigorous analysis by the Norwegian

Institute of Food, Fisheries and Aquaculture Research (NOFIMA) and SINTEF of its resource utilisation and eco-efficiency for the year 2010. Thus Fig. 7 charts the carbon footprint and land occupation by Norwegian farmed salmon and how it compares with Swedish pig and chicken production (when comparing the surface area of the net pen and land use of the salmon feed inputs with the surface area of the land use for the land animal feeds, but excluding the sea primary production area associated with the origin of the marine ingredients).41 Fig. 8 is an overview of nutrient flows and energy use for Norwegian salmon in 2010.12 Key findings were as follows: The carbon footprint of Norwegian salmon was 2.6 CO2e/kg edible product compared with values of 3.4 and 3.9 for Swedish chicken and pig respectively. The land occupation per kg of edible product for Norwegian salmon was 3.32 m2/kg compared with values of 6.95 and 8.35 for Swedish chicken and pig respectively.

Changing the diet composition from 85% plant ingredients to 88% marine ingredients resulted in almost the same carbon footprint, while excluding marine ingredients from South America and the Mexican Gulf from the 2010 diet increased the carbon footprint by 7%. Cumulative energy demand for the Norwegian 2010 salmon was 25.3 MJe/kg , edible product; the ratio of industrial energy input/energy output in salmon product was 3.6/kg liveweight and 6.2/kg edible product respectively. It should be noted that â&#x20AC;&#x2DC;edible productâ&#x20AC;&#x2122; here excludes salmon heads, frames etc., which can be used to produce other forms of edible product or eaten directly by some Asian communities. Producing 1kg of edible chicken and pork requires 2-3 times more phosphorus (as fertilizer) compared with salmon, which retain around twice as much dietary phosphorus. Retention of EPA and DHA was 58% in the whole salmon and 26% in fillet, whereas overall retention of protein and energy was 26% and 21% respectively in the edible part of Norwegian salmon in 2010 (net of losses in feed and salmon production). The NOFIMA study shows clearly that salmon farming in Norway is a more efficient way of producing nutrients for human consumption than chicken and pork production. Farmed salmon retain nutrients more efficiently and are more efficient converters of feed nutrients to human food than pigs and chicken. At the same time it should be noted that LCA of global salmon farming systems showed impacts in most categories were lowest for Norwegian production and that the most critical factor was least-environmental cost feed sourcing.42

Atlantic salmon

Pig

Chicken

Lamb

Table 1. product yield, energy, and protein retention in edible parts of Atlantic salmon, pig, chicken and lamb (Source: Bjorkli 2002) (a) Harvest Yield is yield gutted and bled animal (b) Edible yield is ratio of total body weight that is normally eaten, muscle, body adipose tissue and liver, lung and heart for pig. Skin is excluded for all animals. (c) FCR = (kg feed fed)/(kg body weight gain) (d) Energy retention + (energy in edible parts)/(gross energy fed) (e) Protein retention = (kg protein in edible parts)/(kg protein fed)

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scientific kgCO2e/kg edible product

kg CO2e m2 land

Figure 7. Carbon footprint and land occupation by Norwegian farmed salmon and Swedish pig and chicken Source: Hognes et al, 2011 SINTEF report (see below) Comparison of occupation of agricultural land (top axis) and greenhouse gas (GHG) emissions (bottom axis) from production of 1 kilo edible Norwegian aquaculture salmon and Swedish chicken and pig. From project with SIK:

In this connection it appears that the origin of feed ingredients affects the LCA results and environmental impacts are highly dependent on the reduction fish species used and the energy needed to catch them.43 Of particular interest was NOFIMAâ&#x20AC;&#x2122;s finding that substitution of marine

ingredients by plant ingredients had virtually no effect on carbon footprint. The strong trend towards substitution in salmon feeds is occurring in other aquaculture feeds and has more to do with spreading the supply risk and being less reliant on limited supplies of marine ingredients showing marked

Figure 8. Overview of the nutrient flows and energy use in Norwegian salmon production in 2010. Source: Ytrestoyl et al, 2011 NOFIMA report no. 53/2011 ISBN: 978-82-7251-9451. 65pp

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volatility in costs. There is no evidence that terrestrial agricultural animal and plant feed resources are more sustainable than those from wildcaught marine resources. However, the environmental movement is dominated by marine conservation organisations which pressure fish supply chains to lower the use of marine ingredients for aquaculture diets without considering sustainability issues in regard to alternative ingredients (e.g. rain forest impacts of increased soya cultivation). In addition to the factors considered in the NOFIMA study, plant production requires freshwater, unlike salmon farming (apart from hatchery smolt production), and contributes to depletion of the soil. Most plant ingredients can also be used for human consumption, and the benefit of substituting marine ingredients produced from well managed fisheries supplying fish species for which there is little or no demand for human consumption is not obvious.44 These results are reinforced by the conclusion of Welch et al.33 that farming salmon increased production of animal protein at generally lower land, water, nitrogen and agricultural chemical costs than terrestrial livestock.

7. Farmed and wild salmon: supply chain issues, human nutritional issues, and coproducts In 2012 global supply of farmed salmon (dominated by Atlantic salmon) was 2.1 million tonnes (head-on; gutted) compared with approx. 824 000 tonnes of wild salmon, mainly comprising different species of Pacific salmon.5 Salmon consumption worldwide is over three times higher than it was in 1980 and what was once a luxury food is now among the most popular fish species in the U.S., Europe and Japan. Salmon aquaculture is the fastest growing food production system in the world. To commercial supply chains salmon is a highly versatile raw material in terms of value adding options and product forms (e.g. smoked), as well as having a healthy image in common with other oily fish species linked to its long chain omega3 fatty acid content. When compared with the quality aspects of meat products from land animals, salmon was rated as being superior in healthiness by European consumers.45

scientific These attributes are common to both farmed and wild salmon, but does the farmed product have advantages or disadvantages in the market place compared with wild salmon? Farmed Atlantic salmon products have proved highly attractive to both food service and retail distribution channels. For example in the UK, farmed salmon currently represents the most commonly stocked fish species on supermarket shelves, although smaller volumes of wild Pacific salmon are now becoming available in the UK, albeit at a price premium to the consumer. This reflects the comparative advantage of aquaculture’s control over production compared with wild fish. In particular, wild fish suppliers are unable to match the year-round availability of fresh, frozen and processed salmon with consistent quality from supply chains willing and able to enter into forward contracts for agreed price and quantities. Subjective evidence from blind taste panels suggests that farmed salmon is often preferred to wild salmon; this may, of course, be linked to farmed salmon containing over 30% more fat than wild counterparts and the likelihood that panellists are more acquainted with, and possibly conditioned to, the organoleptic properties of farmed salmon, which is more commonly consumed worldwide. Commercially successful salmon farming (like broiler chicken farming) is all about management of the supply chain to provide continuity of supply. The key steps include raw material procurement, farm management, processing and distribution, while at the same time other supply chain issues include quality assurance and verification that procedures are being followed, including audited verification of Good Manufacturing Practice and HACCP. However, due to consumer concerns about overfishing, a supply chain requirement of growing importance for both farmed and wild salmon is independent third party certification of sustainable sourcing. In the case of wild salmon, certain retailers and food service channels insist the source fishery demonstrates it is being sustainably managed, either by assessment and certification with the Marine Stewardship Council,46 or with the FAO-based Responsible Fisheries Management scheme, which has been adopted by Alaska Fisheries.47 In the case of farmed salmon, various organisations offer independent verification of responsible practice, e.g. Best Aquaculture Practice,48 and more recently the Aquaculture Stewardship

Council.49 In addition the supply of fishmeal and fish oil is addressed by the Responsible Supply standard of the International Fishmeal and Fish Oil Organisation.50 The salmon farming industry in each of the major producer countries has established representative organisations, not only as a political voice, but also in an effort to improve the quality and sustainability of the industry. This has close parallels with the various organisations representing terrestrial livestock industries. Thus in Scotland the Salmon Producers’ Organisation51 is committed to maintaining standards in the industry via the independently audited Code of Good Practice for Scottish finfish aquaculture (covering food safety and consumer assurance; fish health and biosecurity; managing and protecting the environment; fish welfare and care; and feed and feeding).52 Retailers focusing on welfare may also demand other certifications and it is of interest that approx. 70% of Scottish farmed salmon is now certified by Freedom Food53 as achieving high fish welfare standards; this has in turn resulted in higher overall standards of farm practice, while aligning closely with consumer demands for farming systems which strive to care for the animals’ well-being for both terrestrial and aquatic farming systems. Unlike broiler chicken farming, for example, it should be noted that salmon cage systems are open to the environment, hence inherently less biosecure. This in turn aligns with the perception of ‘working with nature’ to resolve problems like sealice control, while at the same time supply chains can claim to be responding to consumer demand for more ‘natural’ food. The emphasis on environmental certifications must not obscure the fundamental objective of producing wholesome and nutritious food in a cost-efficient and safe manner. Salmon is an important source of the nutritionally important PUFAs, for which there is strong demand from the human nutritional sector as well as aquaculture. Man has a limited ability to elongate and desaturate alphalinolenic acid (e.g. from oil seeds) and it is generally recognised that the lack of long chain omega-3 fats in the meat of land animals and the presence instead of more saturated fats, especially of the omega-6 series, can predispose to human health problems (e.g. obesity and cardiovascular disease) if there is inadequate balance

of omega-3 and omega-6 fats54. Traditional poultry and eggs were one of the few land-based sources of long-chain n-3 fatty acids, especially DHA, which is synthesized from its parent precursor, but the evidence is that this has now changed with chickens in the UK market providing several times the fat energy compared with protein and much reduced PUFA levels, hence potentially negative consequences for animal welfare and human nutrition.71 This nutritional health benefit of salmon is shared by other high oil fish, hence adding further value to salmon as a product and a competitive advantage as against land animals. The trend towards high energy salmon diets and the sole use of fish oil as a dietary fat source meant that formerly farmed Atlantic salmon, having a higher fat content than wild salmon, also had a higher content of PUFA than wild salmon, especially when oil-rich fish such as anchovy (Engraulis spp.), herring (Clupea harengus), or sandeel (Ammodytes spp.) were used. Since the progressive introduction of vegetable oils as a partial dietary substitute for fish oil from around the year 2000, and influenced by the growing competition for PUFA-rich fish oils by the human nutrition industry, the content of PUFA in farmed salmon has reduced to only a third of what it was before the year 2000.55 This may undermine the basis of dietary recommendations for human consumption of oily fish; for example, EFSA56 recommends a minimum of 250 mg/day of combined EPA + DHA, whereas the UK (Scientific Advisory Committee on Nutrition)57 recommends a minimum of 450 mg/day of combined EPA + DHA and consuming fish twice a week, including one meal of oily fish. Although different farmed salmon are being reared on different combinations of fish and vegetable oil, it is possible that some wild salmon will now contain more PUFA per gram than some farmed salmon. However, it is clear that product differentiation is now occurring with some supply chains demanding their salmon is supplied with a greater concentration of EPA and DHA than other supply chains. For example, certain UK retailers have focused on maintaining higher PUFA levels in salmon fillets and Scottish producers have contracted to supply this market segment; it is likely that segmentation will become increasingly apparent to consumers in terms of product labelling and premium pricing.55

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scientific Amino acids, % of protein Amino acid

Salmon meal (a)

Salmon hydrolysate (b)

Chicken (c)

Adult human (d)

Schoolchild (d)

Table 2. Comparison of amino acid content in (a) salmonmeal and (b)hydrolysate with requirements of (c) chickens and (d) humans (Ramirez 2007) Sources (a) ww.pesquerapacificstar.cl (b) Wright, 204 (c) Nutrient requirement of poultry, 1994 (NRC) (d) Protein and amino acid requirements in human nutrition, WHO, Technical Report Series [2007(935):1-265]

Given the worldwide scarcity of PUFArich fish oil, this situation is likely to pertain until such time as new costeffective PUFA sources emerge from current research and development using algal production and genetic modification of oilseeds (see 8 (vi)). Not all salmon is eaten directly and salmon coproducts typically represent around 40% of total ungutted carcase weight; such coproducts include aquaculture meals and oils for livestock feeds (which cannot be recycled back into salmon feed to avoid potential health problems), but also a variety of value-added products for use in the human nutritional and pharmaceutical sectors.58 In general the protein quality of fish meat is higher than land animal meat, for example it is higher in lysine and methionine as a proportion of total amino acids. Table 2 compares the amino acid content in salmon meal and hydrolysate with the requirements of chickens and humans (adults and schoolchildren).59 Tryptophan seems to be the only limiting amino acid for all diets although this may be linked to analytical problems. Arginine for poultry seems to be the only true limiting amino acid in salmon meal, but not in the hydrolysate where threonine appears marginally limiting. Farmed and wild salmon contain calcium, copper, iron, magnesium, manganese, phosphorus, potassium, selenium, sodium and zinc. Other micronutrients present include Vitamins A and D and a range of B vitamins, with farmed salmon being much higher than wild salmon in thiamine and folic acid. Clearly the nutritional composition of wild and farmed salmon reflects their feed intake, which reflects the source of their feed. In the case of Norwegian farmed salmon, the marine feed ingredients may include fishmeal and oil from locally available fish (e.g. capelin) and process trimmings from fish for human consumption, as well as imported fishmeal and oil derived from

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species such as Peruvian anchovy (Engraulis ringens). The majority of salmon dietary ingredients are now of vegetable origin, such as soya protein concentrate and rapeseed oil, and likely to be imported into the main salmon producing countries. The efficiency with which salmon convert these feed nutrients to nutrients for human consumption and the superior quality of the output relative to terrestrial livestock have implications for future food security, especially given the static nature of capture fishing.

8. Overcoming technical constraints (i) Off-shore production

A possible alternative to the problems of siting salmon cage farms at inshore locations is moving the production units offshore to deeper and less sheltered waters, where ocean currents are stronger. This avoids the risk that heavily used inshore sites can become progressively unusable despite adopting site rotation and fallowing. At the same time offshore locations avoid many of the conflicts that occur with other marine resource users in the more crowded inshore waters, although user conflicts exist offshore too. This requires sophisticated, capitalintensive cage rearing and feeding systems capable of withstanding open ocean gales; such offshore systems are now being introduced for marine fish and shellfish farming, but are at an early testing phase for commercial salmon farming. (ii) Recirculation and land-based systems

Recirculation technology is showing potential for intensive aquaculture with minimal water consumption60 and is enabling salmon smolt production to take place under environmentally controlled conditions at optimal water

temperatures with minimal bleed-in of freshwater. Marine finfish species are also now being reared intensively in closed circuit, land-based, recirculation units away from the coast, hence potentially avoiding the problems of escapement and biosecurity described in relation to salmon cages, but the key issue is the cost of energy for such systems which may therefore be difficult to scale up commercially. (iii) Genetic improvement

The relatively long generation time of salmon compared with warmwater farmed fish (e.g. Tilapia spp.) means that selective breeding takes longer. However, during the last 40 years genetic progress with Atlantic salmon has markedly improved key production traits. For instance, a near doubling in growth rate has resulted in a reduction in the length of the production cycle to 1.5 â&#x20AC;&#x201C; 2 years;10 the onset of sexual maturation has been delayed; FCR has dramatically reduced; higher survival rates have been achieved (including increased resistance to specific pathogens); and fillet quality has been enhanced in terms of fat and colour. The application to salmon aquaculture of molecular biology techniques (looking at single genes), as well as genomics (looking at DNA sequencing), is set to offer a fundamental approach to solving specific problems. The first Atlantic salmon genome is about to be fully sequenced due to international collaboration61 and early project objectives are to identify the genes for sexual maturation, those that code for sealice resistance, and for preferred meat texture. (iv) Triploids

The use of sterile salmon by farmers would overcome the risk of escaped fish affecting wild populations and two possible routes are being considered: triploidy and genetic modification.

scientific Triploid induction (by shocking the egg shortly after fertilisation) was tested in the 1990s to prevent salmon maturation prior to harvest, but also resulted in poor performance, reduced disease resistance, and deformities and was therefore abandoned in favour of photoperiod control of maturation. It is now recognised that growth and survival of triploid salmon is strongly affected by family. By means of correct selection, triploids were found to outperform their diploid siblings with minimal deformity rates62 and the feasibility of using triploid salmon is again being studied in Norway and Scotland. (v) GM salmon

The use of GM salmon is promoted as a sustainable alternative to conventional salmon farming. Thus trademarked ‘AquAdvantage’ salmon are Atlantic salmon with a gene from chinook salmon (Oncorhynchus tshawytscha) reducing the time to market by 50%. The owners, AquaBounty,63 intend to grow the fish as sterile, all-female fish in land-based facilities. The US Food and Drug Administration is currently considering their application to approve GM salmon for human consumption. If granted this would be the first genetically modified animal allowed to be sold to consumers. Consumers in Europe are unlikely to accept the product. The largest global salmon farming company (Marine Harvest) has recently issued a statement saying that it does not support the introduction of GM salmon and asking for it to be specifically labelled as such in the event that it is approved for consumption. The European salmon farming industry even avoids the use of (authorised) GM ingredients in the

feed.

forward solutions.

(vi) GM feed ingredients

(viii) Feeds

The increased scarcity and cost of fish oil has spurred research into manufacture of long chain PUFAs, especially EPA and DHA, by means of algal production (e.g. by fermentation) and by genetic modification of oilseeds, such as soyabean, rapeseed, and Camelina sativa. Limited quantities of these fatty acids are already commercially available from algal production, while GM material has only been produced experimentally and is some way from commercialisation assuming consumer concerns and regulatory hurdles are overcome. As regards GM soya, canola, and other vegetable protein feed ingredients, these are now being used widely by the aquaculture industry. However, so far, salmon feeds in Europe have not contained GM ingredients due to continuing consumer concerns.

The main challenges to extending substitution of marine ingredients by further dietary inclusion of plant protein and oils is linked to their lower protein and unsaturated omega-3 fatty acid contents and higher starch and fibre contents, unfavourable amino acid profiles, and the presence of antinutritional factors.64 Plant protein and lipid inclusions had reached 40% by 20107 and are now exceeding 50% especially in the case of lipid sources.55 Given the level of research focus by nutritionists and feed formulators, there is little doubt that inclusion levels of plant materials will increase and that marine ingredients will be used more strategically, especially at critical parts of the life cycle, such as in first feeding and smolt transfer diets.65,66 The limiting marinebased nutrients of most concern for salmon performance are certain amino acids (e.g. lysine and methionine) and long-chain omega-3 fatty acids; the latter reflecting the increasing scarcity of suitable fish oil until alternative sources become available (see 8 (vi) above). Although the long-chain omega-3 requirement of salmon is low and likely to be covered in practice by the dietary fishmeal, even in the absence of added fish oil,67 the concern is more about the consumer impact of low levels of EPA and DHA in the resulting end-product. Consumer concerns are also linked to the continued resistance within Europe to using land animal by-products in salmon diets despite the European Commission recently authorising the reintroduction of processed animal proteins from non-ruminant farm animals as feed ingredients (c.f. also resistance to GM materials). However, increased use of plant materials raises its own sustainability issues, since calculations of the hypothetical area required for supplying 100% of all the macro-nutrients from plant sources indicate that Norwegian salmon production would need around 1.1 million hectares (45% of the total agricultural area of Denmark) in order to produce 270 000 tonnes of wheat, 1.56 million tonnes of soya, and 950 000 tonnes of rapeseed7. Much of the soya would presumably come from Brazil and further expansion threatens the southern Amazon basin. Already the soybean trade between Brazil and Europe is creating environmental, social, and economical concerns that have yet to be fully resolved.68

(vii) Stock losses

Currently in Norway one out of five smolts stocked in a cage will not reach the market due to diseases, escapes, and production disorders; reducing these losses would improve animal welfare and also reduce the use of resources.7 The situation in second-placed Chile is substantially worse, due mainly to health problems, and the authorities are now taking steps to reduce the density of farms in a given area and to open up new ‘clean’ sites. Therefore disease prevention and control continues to be of major importance in salmon farming and the intense research focus on priorities, such as sealice, helped by new techniques becoming available, is likely to bring

Interior view of office on feed barge showing monitors for remote cameras and digital display of temperature and dissolved oxygen” (courtesy of Scottish Salmon Producers’ Organisation)

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scientific 9. Conclusions Whereas fishing and land animal production have developed over millennia, large scale intensive aquaculture has only developed over the past 30 – 40 years. Over this same period, issues such as the use of antibiotics, biodiversity, pollution, and animal welfare, have come to the fore in regard to land animal production, especially in developed economies. Salmon farming is the most developed form of intensive aquaculture but from the start it has been subjected to constant critical scrutiny on these issues. That it has not only survived, but grown to be a highly efficient global industry, is mainly due to innovation and rapid technological change enabling increased productivity, cost reduction, and close control of the production process. These factors have enabled the industry to resolve most of its problems, improve its productivity, and succeed commercially on a global scale, while becoming increasingly sustainable. The criticism that salmon farming relies on the unsustainable use of dietary ingredients of marine origin was reviewed in an earlier paper, which explained why the continuing substitution of marine ingredients by vegetable proteins and oils in salmon feed, together with the evidence that reduction fisheries are not being overexploited to produce more and more fishmeal and fish oil, make this criticism increasingly untenable. This review has covered other environmental criticisms of salmon farming, including the impact of its effluent discharge, the use of antibiotics and chemicals, the transmission of disease agents into the marine ecosystem, and the threat to wild salmon populations arising from escaped farmed fish (due either to interbreeding or to disease transmission). During its rapid industrialisation, the industry has had to learn how to address these environmental effects and to evolve codes of good practice in order to avoid reduced productivity, hence reduced profitability, and to comply with government regulations. Improved husbandry knowledge and operating practices, as well as tighter regulatory frameworks, have largely helped the industry to internalise and mitigate these problems in Europe and North America,69,70 with the Chilean industry somewhat lagging behind. Sealice infections and salmon escapes are probably the most serious

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environmental challenges in salmon farming, at least for the dominant Norwegian industry. Intensive research continues to achieve more effective sealice control, including vaccination and the use of live cleaner fish to browse on lice attached to salmon skin. The long term prevention of salmon escapees breeding with wild salmon depends on consumers accepting a switch to farming sterile salmon. Fears that farmed salmon may concentrate environmental contaminants in the flesh and hence pose a human health risk are false. Nor is there evidence to support the view that salmon farming has been responsible for the widespread decline in wild salmon populations in Europe or North America. When compared with wild-caught fish, farmed salmon has a clear ecological advantage. Norwegian studies by NOFIMA have shown that, if the objective is to provide marine nutrients for human consumption, it is far more efficient to harvest pelagic fish for fishmeal and fish oil to rear salmon than to leave them in the sea as prey for cod and instead harvest the cod resource. Using capelin to produce salmon gave nearly 10 times more marine protein and 6 times more long-chain omega-3 fatty acids compared with harvesting the cod, despite farmed salmon and wild cod having comparable LCAs. Overall salmon farming is a more efficient use of resources than commercial fishing, especially when taking account of fishing externalities. In fact the oceans provide an under-utilised source of nutrients for human consumption and salmon farming offers an efficient mechanism for transforming these resources into high quality food that can be distributed worldwide and available all the year round. The NOFIMA study shows that salmon farming in Norway is a more efficient way of producing nutrients for human consumption than chicken and pork production, as indicated by its climatic impact, area of land occupation, and use of non-renewable phosphorus resources. Farmed salmon also retain nutrients more efficiently compared with pigs and chicken, but there is no evidence that terrestrial agricultural animal and plant feed resources are more sustainable for farming salmon than using feed ingredients based on wild-caught marine resources. Although still young, the salmon farming industry has greatly increased the availability and reduced the cost of

supplying salmon to world seafood markets. It has also brought sustainable employment to many remote rural locations. The main challenge going forward will be to continue to grow sustainably in step with market and environmental considerations. A major priority is the reduction in losses over the production cycle of around 20% of fish stocked into a cage. Also sealice infestation and escaped salmon must be better controlled. A potential limiting factor is the availability of PUFAs due to growing competition for fish oil from the human nutrition industry. It will be necessary to increase further the proportion of plant oil (mainly rapeseed oil) in salmon feed, hence reducing the EPA and DHA levels in the fillet, which might adversely impact consumer demand; but in due course this will be solved when cost-effective material becomes available either from algal manufactured oils or from geneticallymodified plants. It will be of interest to consider whether valid comparisons can be made between salmon farming and other types of aquaculture, including less intensive systems, especially as regards environmental impact and resource use. The answers to such questions may help us to draw conclusions on the potential role of global aquaculture for future food production and food security.

Acknowledgements The authors gratefully acknowledge the advice and assistance of Petter Arnesen, Frank Asche, Ragnar Nystøyl, Randoph Richards, and John Webster. Special thanks are due to Torbjørn Åsgård and Trine Ytrestøyl (NOFIMA) and to Erik Skontorp Hognes (SINTEF), and their respective colleagues, whose work on the Norwegian salmon industry features extensively in this review.

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account in chicken, pig and lamb). Master’s thesis at Agricultural University of Norway (in Norwegian). 40. Åsgård T and Austreng, E (1995) Optimal utilization of marine proteins and lipids for human interest. In Reinertsen & Haaland (Eds.): Sustainable fish farming. Balkema, p 79-87 41. Hognes, E S, Ziegler, F, and Sund, V (2011) Carbon footprint and area use of farmed Norwegian salmon. SINTEF report no F21039. SINTEF Fisheries & Aquaculture, Trondheim, Norway, 30 pp 42. Pelletier, N, Tyedmers, P, Sonesson, U, Scholz, A, Ziegler, F, Flysjo, A, Kruse,S, Cancino, B and Silverman, H (2009) Not All Salmon Are Created Equal: Life Cycle Assessment (LCA) of Global Salmon Farming Systems. Environmental Science & Technology, 43, 8730-8736. 43. Boissy, J, Aubin, J, Drissi, A, van der Werf, H M G, Bell, G J and Kaushik, S.J, (2011) Environmental impacts of plant-based salmon diets at feed and farm scales. Aquaculture 321, 61-70 44. Wijkström, U N (2012) Is feeding fish with fish a viable practice? In Farming the Waters for People and Food (Subasinghe, R P, Arthur, J R, Bartley, D M, De Silva, S S Halwart, M, Hishamunda, N, Mohan, C V and Sorgeloos, P, eds). Proceedings of the Global Conference on Aquaculture 2010, Phuket, Thailand. 22-25 September 2010. pp. 33-35. FAO, Rome and NACA, Bangkok. 45. Onozaka, Y, Hansen, H, and Tveterås, R (2012) Salmon’s position among consumers. Global Aquaculture Advocate, Vol 15, Issue 5, September/October, pp. 68-70 46. Marine Stewardship Council (2013) http://www.msc.org/get-certified?gclid=CLX2ZG36bsCFWbLtAodqVcAgg 47. Alaska Seafood (2013) http://certification.alaskaseafood.org/fao-based 48. Global Aquaculture Alliance. http://www.gaalliance.org/bap/standards.php 49. Aquaculture Stewardship Council www.ascaqua.org 50. International Fishmeal and Fish Oil Organisation www.iffo.net/iffo-rs-standard 51. The Scottish Salmon Producers’ Organisation www.scottishsalmon.co.uk 52. Code of good practice for Scottish finfish aquaculture www.thecodeofgoodpractice.co.uk 53. RSPCA Freedom Food http://www.rspca.org.uk/freedomfood 54. Simopoulos, A P (2008). The importance of the omega 6/omega 3 fatty acid ratio in cardiovascular disease and other chronic diseases. Experimental Biology and Medicine, 233(6):674-688 55. Shepherd, C J (2012) Implications of increased competition for fish oil. Bergen. FishFarmingXpert, September 2012. 15:40-45 56. European Food Safety Authority (2009) Scientific Opinion: Labelling reference values for n3 and n-6 polyunsaturated fatty acids. EFSA journal 1176, 1-11. http://www.nutraingredients.com/Regulation/EFSA -proposes-reference-intake-levels-for-omega-3omega-6. 57. Scientific Advisory Committee on Nutrition. (2004) Advice on fish consumption, benefits and risks. http://www.sacn.gov.uk/pdfs/fics_sacn_advice_fish .pdf 58. Newton, R, Telfer, D and Little, D C (2014) Perspectives on the utilisation of aquaculture coproducts in Europe and Asia; prospects for value addition and improved resource efficiency. Critical Reviews in Food Science and Nutrition 54:495-510 59. Ramírez, A (2007) Salmon by-product proteins. FAO Fisheries Circular. No.1027. Rome, FAO. http://www.fao.org/docrep/010/a1394e/a1394e0 0.HTM 2007. 31p.

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scientific 60. Costa-Pierce, B A, Bartley, D M, Hasan, M, Yusoff, Y, Kaushik, S J, Rana, K, Lemos, D, Bueno, P and Yakupitiyage, A (2012) Responsible use of resources for sustainable aquaculture. In: Farming the Waters for People and Food. Proceedings of the Global Conference on Aquaculture 2010 (R P Subasinghe, J R Arthur, D M Bartley, SS De Silva, M Halwart, N Hishamunda, C V Mohan and P Sorgeloos. eds.), FAO, Rome and NACA, Bangkok, Phuket, Thailand. 22-25 September 2010. pp.113147. 61. International collaboration to sequence the Atlantic salmon genome http://www.genomebc.ca/files/2912/6929/4134/5 .2.2%20dec7%20background.pdf 62. Migaud, H (2013) Pers. Comm. 63. AquaBounty http://www.aquabounty.com/products/products295.aspx

64. Hemre, G I, Karlsen, O, Mangor-Jensen, A, Rosenlund, G (2003) Digestibility of dry matter, protein, starch, and lipid by cod (Gadus morhua): Comparison of sampling methods. Aquaculture, 225:225-232 65. Jackson, A J and Shepherd, C J (2010) Connections between farmed and wild fish: fishmeal and fish oil as feed ingredients in sustainable aquaculture. In: Advancing the aquaculture agenda. Policies to ensure a sustainable aquaculture sector. Organisation for Economic Cooperation and Development. Paris,15–16 April 2010, pp. 331–343 66. Tacon, A G J, Hasan, M R and Metian, M (2011) Demand and supply of feed ingredients for farmed fish and crustaceans: trends and prospects. FAO Fisheries and Aquaculture Technical Paper No.564. FAO, Rome, Italy. 87pp. 67. Turchini, G M, Torstensen, B E and Ng, W-K

(2009) Fish oil replacement in finfish nutrition. Rev. Aquaculture 1, 10-57 68. Cavalett, O and Ortega, E (2009) Energy, nutrient balance, and economic assessment of soybean production and industrialisation in Brazil. J. Cleaner Product. 17:762-771 69. Asche, F, Guttormsen, A G and Tveterås, R (1999) Aquaculture – opportunities and challenges. Marine Resource Economics 23: 395400 70. Tveterås, S (2002) Norwegian Salmon Aquaculture and Sustainability: The Relationship between Environmental Quality and Industry Growth. Marine Resource Economics, 17, 121-132 71. Wang, Y,; Lehane, C, Ghebremeskel, K; Crawford M.A.(2010) Modern organic and broiler chickens sold for human consumption provide more energy from fat than protein. Public Health Nutrition, 13 3, 400-408.

Collecting salmon by well boat for harvest – note the net has been pulled up to crowd fish around the pump (courtesy of Ian Armstrong)

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the GM debate

Pros and cons of GM crops as a source of resistance to insect pests Professor Helmut van Emden School of Agriculture, Policy and Development, The University of Reading, Earley Gate, Reading, Berks., RG6 6AR, United Kingdom Summary Current experience of the pros and cons of using GM crops for resistance to insect pests is largely limited to one source of transgene, the proteins expressing the toxin of Bacillus thuringiensis. Since the gene transferred, and not the method of transfer, is relevant to the topic of this paper, we can explore what is known from plants traditionally bred for insectresistance based on similar mechanisms to those likely to be used in GM crops, i.e. on single toxins giving a high level of control. Across a whole range of potential issues including the development of pest strains tolerant to the toxin and sideeffects on natural enemies, crops with resistance mechanisms based on high concentrations of toxins compare badly with crop varieties giving partial and more broadly-based resistance. Such partial resistance may, however, be fully effective when integrated with biological control and selective use of pesticides. However, it must be pointed out that this is not the comparison that matters, for GM crops will not be used to replace other forms of plant resitance, but instead to replace insecticides. In that comparison, the replacement of the spraying machine by a GM crop as the vehicle for delivering toxins has clear advantages. Keywords genetically modified crops, human safety, insecticide resistance, natural enemies, plant resistance, tolerance, yield loss.

Abbreviations

Bt Bacillus thuringiensis; DIMBOA 2,4 dihydroxy 7 methoxy 1,4-benzaxazin-3-one; GM genetically modified; IPM integrated pest management; USA United States of America.

Glossary Allelochemical: A chemical produced

by a living organism which, when contacted by another living organism, has deleterious effects on the latter. Cisgene: Transgene transferred between organisms not too distantly related.

Introduction

he term ‘genetically modified’ (GM) has become associated with one particular type of GM, namely direct gene transfer. Rather similar is the way ‘organic farming’ has become associated with that type of farming seen as a contrast with ‘conventional farming'. I make this point because GM has been around since the dawn of agriculture, how else did man progress from wild grasses to productive modern cereals? ‘Traditional’ plant breeding, acceptable to the opponents of ‘GM’, is certainly GM by any definition than other that it does not involve direct gene transfer. Focusing on the technique of gene transfer rather than the properties of the gene transferred is well expressed by the following quotation: “We have recently advanced our

Secondary (plant) compounds:

Synthesised gene: A gene with at least

Complex chemicals made by plants but not essential to the life of the plant.

part of its DNA created artificially. Transgene: Gene transferred from one organism to another by any method. Yield drag/penalty: Reduction in crop yield caused by the diversion of photosynthesis for other purposes such as synthesis of toxins by a plant.

Sink (in relation to photosythesis in plants): A function in the plant creat-

ing a demand for the products of photosynthesis. knowledge of genetics to the point where we can manipulate life in a way never intended by nature. We must proceed with the utmost caution in the application of this new found knowledge”. The fear of something ‘unnatural’ is clearly behind the opposition to GM crops. But doesn’t this exactly make my point that we should concentrate on the gene rather than the method of transfer? Until recently one could avoid the ambiguity of GM by calling direct gene transfer ‘transgenic’, but recently the antonym ‘cisgenic’ has been proposed for the direct transfer of genes amenable to traditional breeding in an effort to find a form of GM acceptable to the ‘organic’ lobby. While this might appear to be retreat, concentrating on the ’naturalness’ of the gene may in the end achieve acceptance that the method of transfer is not very relevant. After all, it is not

possible to limit the genes transferred by breeding to the one(s) desired; there is associated genetic baggage which, if it includes undesirable characters, may take many further cycles of breeding to eliminate; by contrast cisgenics will transfer only what is intended. Incidentally, it is salutary to realise that the quotation above does not relate to ‘GM’ as we understand it today. It expresses the concerns of the agriculturalist Luther Burbank in 1906 when he discovered Gregor Mendel’s work with round and wrinkled pea seeds! The first reference I can find to using transgenic methods to obtain plant resistance to insect pests is in 1979 (1), and it is clearly taking longer for ‘GM’ to be generally acceptable than applied to Gregor Mendel’s work. ‘GM’ crops have now been grown on a large scale since 1996, and the fear of ‘Frankenstein’ consequences does not appear to have any justification.

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the GM debate

Figure 1. How the perceived advantages (left) of transgenic host plant resistance to insects have the potential for disadvantageous side effects (right)

Much of the GM hectarage is planted to insect-resistant crops expressing Bacillus thuringiensis toxins (Bt); this first exploitation of ‘GM’ therefore was for resistance to insects. Since then, genes for a number of other insecttoxic proteins (including lectins, amylase inhibitors, trypsin inhibitors, protein inhibitors, chitinases and cytokinins) have been directly transferred to crop plants, but no commercialisation has as yet followed. If we focus on genes rather than the transfer method, the traditional plant breeding literature provides a great deal of relevant experience about the potential pros and cons of pestresistant GM crops. Key to this is that resistance to pests in GM crops is likely to be based on toxins, and commercial 'GM' varieties will only come to market if the genes express these toxins at a high enough level to give control equalling that given by insecticides. So traditionally-obtained plant resistance can be directly comparable if it is based on a strong toxin. Overdosing is not limited to agrochemicals, and doing it with genes for plant resistance will have consequences not dissimilar from overdosing with insecticides. Recently a trial of GM wheat with a synthesised gene (resynthesised from peppermint to eliminate inhibitory compounds) expressing the alarm pheromone of aphids (2) was carried out. The aim was partly to make the point that GM crops could involve genes whose 'escape' from the trial Chemical (units)

Plant

field could not cause ecological mayhem, but such 'behavioural' and target-specific possibilities are bound to be extremely rare in comparison with toxins. The advantages of ‘GM’ perceived by the agricultural industry are the transfer of single genes without other genetic material, that it is possible to avoid the crossing barriers that exist between unrelated organisms and that the level of expression can reach virtual immunity. Examples from traditional plant breeding involving toxins show us that these advantages also translate to potential disadvantages (Fig. 1) and this is the theme of this article.

Safety for humans Much of the history of the genetic modification of wild plants over past centuries, for most of that time without any understanding of Mendelian ratios, was to reduce dramatically the levels of toxins in those wild plants to make them palatable or even safe to eat. As far as these same compounds conferred resistance to insects, so the susceptibility to pests of the crops increased and we now go back to the wild ancestors to recover these sources of resistance (Table 1 compares the levels of two toxic chemicals in crops and related non-cultivated plants).. Good examples are in the Solanaceae, where wild potatoes and tomatoes are Quantity

Reference 31

Table 1. Quantities of some allelochemicals in cultivated (C) and wild (W) tomatoes and brassicas/

54 WORLD AGRICULTURE

both highly toxic to humans. Safety for humans is paradoxically the one area of potential concern where ‘GM’ crops probably have the advantage. Because of the ‘unnatural’ angle, no one has queried the necessity for ensuring human safety. The Bt toxin was chosen for the socalled ‘first generation’ GM crops specifically for its safety to humans stemming from differences between humans and insects at the cell molecular level. GM crops are subject to stringent testing to ensure safety to humans before they can be marketed. In this they differ from new cultivars obtained by traditional breeding, and they have never been required to undergo similar testing before release. A famous example of the consequences of this is the release in the USA of the potato variety ‘Lineup’, which contained elevated levels of a glycoaldehyde to confer resistance to Colorado beetle (Leptinotarsa decemlineata). Consumers found the flavour of ‘Lineup’ distasteful, and some showed symptoms of toxicity; the new variety had to be withdrawn (3). With GM crops, the public is protected against health issues. A further advantage is that the pest receives the toxin through the plant and not through a chemical spray hazardous to the person applying it.

Yield drag It is hard to think of a mechanism of plant resistance to insects that does not involve some energetic cost to the plant and therefore a potential reduction in yield. Gershenzon (4) has quantified the costs of some compounds involved in plant resistance to insects and, when expressed as per cent of photosynthesis, some costs appear dramatic. For example, production of the triterpene papyriferic acid in birch involves a 24.5% cost, and the flavonoid apigenin (in Isocoma acradenia) a cost of 6.9%. The photosynthetic costs of other compounds cited are lower and mostly range between 0.1 and 4.8%. However, the real costs of producing many of such so-called ‘secondary compounds’ (or ‘allelochemicals’) are nowhere near as great as Gershenzon and many other authors including myself (3) have suggested in the past. Firstly photosynthesis is ongoing whereas production of allelochemicals is not, and secondly radiation is mostly sufficient for photosynthesis to be sink rather than source limited – i.e. the cost of allelochemical production can

the GM debate be compensated for by a rise in photosynthetic rate (4). Thus, referring back to Table 1, the high glucosinolate levels in Sisymbrium officinale can be achieved in only 7.5 minutes of photosynthesis, and the levels of 2-tridecanone in wild tomato take less than one hour (4). Such short times would be typical for annual crops rather than for perennials which make lifetime investments in much more energy-expensive defence compounds such as lignin and tannins that may accumulate to 20% of dry matter. It is therefore not surprising that yield penalties of plant resistance have been hard to demonstrate, including for the quite complex molecules of the Bt toxins. Any potential for yield loss will of course be minimised if partial plant resistance is combined with other pest control methods (Integrated Pest Management or IPM) in contrast with the sole reliance on an allelochemical as is characteristic of GM. However, the latter resistance does have one advantage. In the modification process it may be possible to add promoters which result in the transgenically transferred toxin only being expressed if induced by pest attack. Therefore there can be no yield penalty of the resistance in the absence of the pest.

Tolerant pest strains It is a familiar scenario that continued use of an effective insecticide eventually leads to it losing that effectiveness because pest strains in the population are selected that are tolerant (resistant). Such ‘breakdown of control’ is also very familiar to plant pathologists using resistant varieties to control plant disease organisms such as rust fungi in cereals. With plant resistance, such breakdown is most frequently associated with single major genes for resistance, usually providing only what is known as ‘race-specific resistance’. It is therefore only to be expected that the high selection pressure on a pest imposed by a single effective transgenically transferred toxin will similarly result in ‘breakdown’. In a study of 77 reports from eight countries in five continents (6), more than 50% resistance to Bt crops was found in five out of 13 pest species in 2-011, compared with only one in 2005. In the laboratory, it has been possible to select one of the cotton bollworms (Pectinophora gossypiella) for resistance to Bt cotton in only 10

generations. The widespread expectation of the breakdown of GM pest resistance has led to attempts to checkmate this development by requiring farmers to maintain areas of non-GM cotton to act as ‘refugia’ where moths with some resistance to Bt can mate with susceptible ones. With scientific opinion originally divided on the merits of this approach, this programme was itself an experiment, but does seem to have worked pretty well where the strategy has been implemented. Whereas growing Bt cotton with the strategy in Arizona has shown sustained susceptibility in pink bollworm (Pectinophora gossypiella), control failures without the strategy have been reported in China and India (7). The danger of breakdown of resistance with GM crops stems from the high selection pressure the expression of the gene puts on the pest population and so applies equally to traditional plant resistance based on highly effective allelochemicals – the mode of transfer of the gene is irrelevant! An example of such breakdown in traditional plant resistance is that of monogenic resistance in rice to brown planthopper (Nilaparvata lugens) developed at the International Rice Research Institute in the Philippines. One new variety (IR26) was particularly resistant to the planthopper, but was defeated within only 2-3 years by the appearance of a strain that was tolerant to the resistance (8). By contrast, many examples of plant resistance which are not so strong, are multigenic and/or based on non-allelochemical methods such as tissue hardness, have lasted for many years. As an example, the rootstocks of the vines of old French communion wines, taken to the USA by early settlers from Europe, were grafted in the early 19th century with scions of vine varieties then current in Europe to deal with the destruction being wrought by an aphid (Phylloxera). The resistance this provided is still largely effective today after 200 years, though a tolerant Phylloxera did appear in a small area in Germany in 1994 (9). Indeed, in a review of the literature in 1996 (3) I was only able to find 16 pest species in which resistance-breaking strains had been identified; moreover, several were examples of selection in the laboratory rather than in the field. As mentioned earlier, traditional breeding contrasts with GM in resulting in the transfer of a genetic package which includes the desired gene amongst others, and so

the resistance may not be monogenic if other unknown genes also confer some resistance. Thus resistance to aphids in cereals, thought to be monogenically based on just one compound (the 1,4-benzaxazin-3-one glycoside DIMBOA), involves other resistance mechanisms also (10).

Problem trading One of the advantages the industry claims for GM crops with plant resistance to pests is that it is environmentally preferable to the heavy use of insecticides it replaces. Again, there is nothing special here about GM; the advantage could equally be claimed for traditionally bred resistant varieties. However, an insecticide usually controls more pest species on the crop than the one target organism, and so another pest may build up in numbers and become a new problem once insecticide pressure on the crop is relaxed. This has actually happened in Bt cotton with leafhoppers emerging from little to major economic importance (11).

Damage to beneficial insects Whatever the mechanism of transfer of a gene conferring high expression of a toxin, natural enemies will lose their food supply unless the crop also hosts alternative prey not affected by the toxin. In relation to implementing IPM on crops, there is of course no mileage in trying to combine different methods of pest control if any one of the methods is effective on its own. Toxins in plants, whatever their origin or method of triansfer, are also likely to affect natural enemies directly if they eat poisoned prey on the plants. There are plenty of examples where chemical defence, whether in wild or cultivated plants, also proves toxic to predators and/or parasitoids; some of these are listed by van Emden (12). Allelochemicals are important in soybean varieties bred for resistance to pests and such varieties are known to affect natural enemies adversely (13). One interesting case – sadly probably a rare exception – where high levels of allelochemicals are actually less damaging than lower levels is that of the aphid-resistance factor DIMBOA in wheat. At high levels, the effect on aphids is not acute toxicity, but to deter their feeding. The ladybird predator Eriopis connexa is therefore not as badly affected as it is when eating aphids poisoned on

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Figure 2. Some examples of the outcome of combining host plant resistance to insects with biological control (histograms show the proportion of insects “surviving” the control measures). Histograms in each block from left to right: plant resistance alone (black), biological control alone (checkerboard), prediction of control given by the combination (white), actual outcome (striped). Note: the second block of histograms form the left illustrate negative interaction and the example of diamond-back moth (far right) show simple additivity of the two control measures. More detail of the pest species and sources of the data can be found in (12).

cultivars with lower DIMBOA levels (14). The few toxins so far exploited for transgenic transfer to crops have of course been tested for any deleterious side effects on natural enemies of feeding on prey on such plants. Much of this work relates to Bt, and a review in 2004 (15) of some 25 laboratory and field studies concluded Bt crops would present few problems, and this has been confirmed in more recent studies (e.g. 16, 17). One rather inconclusive laboratory study did suggest high mortality of lacewing larvae when fed caterpillars reared on Bt maize (18). In fact, Bt is rather selective in which taxa it affects, and honey bees are not affected (19, 20). Also, there appears to be considerable dilution through the trophic levels (21). The concentration of 21.7 µg g-1 fresh weight of a Bt toxin (Cry3Bb 1) in maize reduced to 5.6 µg g-1 in mites feeding on the maize, and was reduced further to about 4.5 and only 1.4 µg g-1 respectively in larvae and adults of a predatory staphylinid beetle. Other transgenes proposed for pest resistance seem to pose greater problems in relation to beneficials. The ladybird Adalia bipunctata fed aphids reared on the leaves of potatoes expressing the snowdrop lectin showed no acute symptoms, but female longevity was reduced by half and fecundity by 20-40% (22). Lectins are also toxic to bees (20). Amylase and protease inhibitors proposed for GM legumes against bruchid beetles have been tested against their parasitoids with conflicting results (23, 24); harmful affects cannot be discounted. The high efficacy of pest resistance in

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GM crops makes it difficult if not impossible to exploit the often positive interaction between plant resistance and biological control, whether with indigenous natural enemies present in the agroecosystem or augmented artificially (e.g. by release). These interactions include highly specific ones such as the switch of Cryptolaemus ladybirds from nectarfeeding to carnivory on cotton varieties on which plant breeding has eliminated the extra-floral nectaries on the leaves (25) and the improved predation of aphids by adult ladybirds on the so-called ‘leafless’ pea varieties with a profusion of leaf-substituting

tendrils. These substitute for leaves and afford ladybirds a goodgrip, whereas they frequently fall off the smooth waxy leaves of normal varieties (26). However, positive synergism between plant resistance and biological control is a widespread and much more general phenomenon (3) than the two examples above might suggest , though it cannot be taken for granted (e.g. the examples based on toxins cited above). Positive synergism may arise from numerical relationships, i.e. the predator/parasitoid prey ratio is higher on partially resistant than on more pest-susceptible varieties. This occurs particularly when the natural enemies use host plant cues (especially odours) in searching for prey from a distance. Parasitoids often emerge with a preference for the odour of the host plant (species and even variety) on which they themselves developed (e.g. parasitoids of aphids – (27)). Furthermore the plant odour changes where sucking insects have probed, which enables the parasitoids to home in on the location of even a few prey (as is only to be expected on resistant plants). Thus biological control in Africa of the cassava mealybug by its parasitoid Epidinocarsis lopezi is primarily achieved when the prey are already at very low numbers in the dry season. More usually, perhaps, the positive synergism between partial plant resistance and biological control

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Figure 3. The concentration of different insecticides (listed on left) needed on a partially resistant crop variety to achieve 50% mortality expressed as a percentage of the concentration needed on a susceptible variety. Key to pests: hoppers (checkerboard), aphids (white), Lepidoptera (black), Coleoptera (x striped). More detail of the pest species and sources of the data can be found in (12).

the GM debate

Figure 4. Effect of the allelochemical 2-tridecanone on mortality of bollworms (Helicoverpa zea) from the insecticide carbaryl. Left, comparison between a susceptible (red) and a resistant (red) variety of tomato; right, comparison between two artificial diets – one without (red) and the other with (red) added 2-tridecanone (data from (31).

depends on functional responses, i.e. there is a greater impact per individual predator on resistant than susceptible varieties. The common phenomena (12) appear to be: 1) Prey on resistant plants tend to be smaller – predators will therefore consume more before they are satiated. 2) Smaller prey are also less likely to escape by running away or kicking at the natural enemy. 3) Disturbance by predators/parasitoids may cause the

prey to fall from the plant in greater numbers on resistant than on susceptible plants (eg. 28). 4) Higher pest densities on the leaves of susceptible plants may leave more wax, faeces, honeydew etc. which may impede the movement of natural enemies or cause them to devote searching time to cleaning. A simplistic but nonetheless adequate approach to measuring synergism is that of multiplying the survival coefficients of the synergising components. If, in a given time interval, biological control reduces a pest population by 10% (i.e. survival coefficient = 0.9), the population on a plant with 20% resistance (i.e. survival coefficient = 0.8) should be 0.9 x .08 = 0.72 = 72% of that on the susceptible variety without biological control. Fig. 2 shows this calculation (expressed as percentages) applied to a range of data from the literature (12). Thus there is a potential in IPM for exploiting positive synergism between plant resistance and biological control which is unlikely to be available with GM crops or with traditionally bred resistant varieties expressing similarly high levels of allelochemicals.

Resistance to insecticides The toxicity of insecticides, whether to insects or humans, is measured as dose of active ingredient per unit body weight. Therefore, as insects on resistant

Figure 5. Theoretical insecticide concentration/insect mortality response curves for a pest (herbivore) and a natural enemy (carnivore) on a susceptible crop variety (A) and on one where 50% mortality of the pest (LC50H) is obtained at only 2/3 of the concentration needed on the susceptible variety (B). LC50C, concentration needed to obtain 50% mortality of a natural enemy; striped area, the ‘selectivity window’ (where the proportion of the pest killed is higher than that of the natural enemy).

plants are usually smaller than on susceptible plants, it would be surprising if the same dose of chemical did not kill a higher proportion. There are many examples illustrating this phenomenon (e.g. Fig, 3), but the effect is usually greater than predicted from the reduction in body weight alone; a greater ‘physiological’ sensitivity also seems to be involved. In fact, Fig. 3 suggests that the concentration of pesticide applied to susceptible plants to kill 50% of the pests (LC50) could be reduced by more than one-third on the compared resistant plants (12). However, there are equally examples where pests on resistant varieties have increased resistance to insecticides. The explanation appears to be that exposure to allelochemicals in plants induces an increase in enzymes which can detoxify these chemicals, but also other toxins (including insecticides). This effect has been shown convincingly with the bollworm Heliothis virescens on cotton varieties with a high gossypol content (29) and by measuring the activity of one such detoxifying enzyme (·-naphthyl esterase) in armyworms (Spodoptera frugiperda) fed on eight crop plants known to contain toxic allelochemicals (30). Finally, there was a reduction in mortality from the insecticide carbaryl on resistant (with high levels of 2tridecanone) compared with susceptible tomato plants (31), with almost identical mortalities when the varieties were replaced respectively with artificial diet + 2-tridecanone and standard artificial diet (Fig. 4). Similarly, addition of the glucosinolate sinigrin to an artificial diet increased the tolerance of diamond back moth (Plutella xylostella) progressively between 0 and 0.125 µmol sinigrin g 1 diet (32). Thus on crop varieties with high levels of allelochemicals, whether transgenically or traditionally “bred”, the pests may show resistance to insecticides should these have to be used as, for example, if individuals tolerant to the plant resistance appear in the population. However, there is a further disadvantage of such varieties in relation to insecticides. It was pointed out above that, on many pest-resistant varieties traditionally bred, a lower dose of pesticide will give the same level of control as on a susceptible variety. Those lower doses will, of course, achieve a reduction in the kill of natural enemies – immediately the selectivity of the pesticide application

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on two wheat cultivars, the aphidsusceptible Maris Huntsman and the only partially resistant Rapier. Not only were the doses for the carnivores not reduced by the plant resistance, they were actually somewhat increased, particularly for the ladybird.

Conclusions Table 2. Laboratory estimates of the toxicity of the insecticide malathion to the aphid Metopolophium dirhodum and to two of its natural enemies (the parasitoid Aphidius rhopalosiphi and the larva of the coccinellid Coccinella septempunctata) when reared on the aphid-susceptible wheat cv. Maris Huntsman and the partially resistant cv. Rapier. LD50 and LD90, the dose needed to kill respectively 50 and 90% of the insects. In each pair of figures, the one showing greater tolerance to malathion is emboldened.

in favour of the natural enemies will improve. This is pure IPM! However, there is more to it than that, since this increase in selectivity will be far greater than one might at first envisage. Over 30 years ago, a fundamental difference in the response to insecticides of herbivores and carnivores was identified (33). The former have evolved to cope with allelochemicals in the plants they feed on by producing detoxifying enzymes. Genetically, individuals will differ in their ability to do this. This will result in a large difference in the insecticide concentration required to kill the most resistant compared with the most susceptible individual (Fig. 5A). By contrast, carnivores, feeding on prey which has largely dealt with any toxins in the plant, have less need for any armoury of detoxifying enzymes, and

so there will be less spread in the pesticide concentration needed to kill different individuals (Fig. 5A). Fig. 5B shows how the selectivity window for the natural enemy increases dramatically as pesticide concentration is reduced when only the response of the herbivore is affected. However, exploiting this phenomenon will be difficult in those countries which legislate against deviating from the manufacturerâ&#x20AC;&#x2122;s recommended dose. The theory behind Fig. 6 has been tested in the laboratory (34), using the cereal aphid Metopolophium dirhodum as the pest with the parasitoid Aphidius rhopalosiphi and larvae of the ladybird predator Coccinells septempunctata as natural enemies. Table 2 gives the doses for the pesticide malathion required to kill 50% and 90% of the respective insects

Table 3. Comparison of transgenic host plant resistance to insects with plant resistance obtained by traditional plant breeding and with the use of insecticide. Comparisons favourable to transgenic resistance are italicised.

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Genetic engineering of plant resistance to insects has relied on the direct transfer of single genes for the production of allelochemicals deleterious to plant-feeding pests.to the point of virtual immunity. It is not difficult to find potential disadvantages of this approach, but it must be remembered that insect-resistant GM crops are only commercial because they control serious pest problems effectively. Therefore it is nonsense, as the media and public so often do - to compare them with doing nothing in the way of pest control â&#x20AC;&#x201C; for that is hardly an option. GM crops do have disadvantages (Table 3) when compared with plant resistance obtained by traditional plant breeding, especially since the lower control efficacy usually provided by these can often synergise with biological control and/or limited use of pesticides to give grower-acceptable pest control. How can any synergism occur if one of the methods involved gives total control on its own? Of 13 mechanisms of plant resistance developed by traditional plant breeding (34), only three involve allelochemicals. Some progress with GM is being made in making the expression of the allelochemical dependent on pest attack occurring, and in transferring more than a single gene for resistance, but the single gene usually giving constitutive protection is still the norm. However, in nearly every case, a pestresistant GM crop will be used to replace (usually heavy) insecticide applications. This is therefore the most important comparison, and GM crops clearly have major advantages (Table 3), particularly in terms of human safety, in selectivity in favour of natural enemies and less environmental contamination. In general, natural chemical compounds are more easily and rapidly broken down to harmless compounds in the environment than are synthetic ones. Perhaps pestresistant GM crops would get a better press and be more readily accepted by the public if they were viewed as an alternative to the spraying machine as a way of delivering insecticide!

the GM debate References 1. Levin, B R (1979) Problems and promise in genetic engineering in its potential applications to insect management. In: Genetics in relation to pest management (eds M A Hoy & J M McElvey, Jr), New York, Rockefeller Foundation, pp. 170175. 2. Bruce, T J A, Smart, L E, Aradottir, G J, Martin, J L et al. (2011) Trangenic wheat emitting aphid alarm pheromone. (E)-beta-farnesene, Aspects of Applied Biology, 110, 112. 3. van Emden, H F (1996) Host-plant resistance to insect pests. In: Techniques for reducing pesticide use (ed. D Pimentel), Chichester, Wiley, pp. 130152. 4. Gershenzon, J (1994) The cost of plant chemical defense against herbivory. A biochemical perspective. In: Insect-plant interactions, vol. 5 (ed. E A Bernays), Boca Raton, CRC Press, pp. 173-205. 5. Foyer, C H, Noctor, G. & van Emden, H F. (2007) An evaluation of the costs of making specific secondary metabolites; is the yield penalty incurred by host plant resistance to insects due to competition for resources? International Journal of Pest Management, 53, 175-182. 6. AFP (2013) ‘More pests resistant to GM crops’: a study <http://www.google.com/hostednews/afp/article/ ALeqM5gkQ3lN4hx0r59smxAQgaWzlWKaVg> accessed 10 03 2014. 7. Tabashnik, B E, Morin, S, Unnithan, G C, Yelich, A.J. et al. (2012) Sustained susceptibility of pink bollworm to Bt cotton in the United States (special issue on insect resistance). GM Crops, 3, 194-200. 8. Panda, N & Khush, G S (1995) Host-plant resistance to insects. Wallingford, CAB International. 9. Anon (1994) Die Rükkehr der Reblaus. Profil, October 1994, 11. 10. Gallun, R L (1977) The genetic basis of hessian fly epidemics. In: The genetic basis of epidemics in agriculture (ed. P R Day). Annals of the New York Academy of Sciences, 287, 1-400. 11. Steinkraus, D C, Young, S Y, Gouge, D H] & Leland, J E. (2007). Microbial insecticide application and evaluation: Cotton. In: Field manual of techniques in invertebrate pathology, 2nd edn. (eds L A Lacey & H K Kaya), Dordrecht, Springer, Section VII-6. 12. van Emden, H F (1999) Transgenic host plant resistance to insects – some reservations. Annals of the Entomological Society of America, 92, 788797. 13. Boethel, D J (1999) Assessment of soybean

germplasm for multiple insect resistance. In: Global plant genetic resources for insect-resistant crops (eds S L Clement & S S Quisenberry), Boca Raton, CRC Press, pp. 101-129. 14. Martos, A, Givovich, A & Niemeyer, H (1992) Effect of DIMBOA, an aphid resistance factor in wheat, on the aphid predator Eriopsis connexa Germar (Col.: Coccinellidae). Journal of Chemical Ecology, 18, 469-479. 15. Schuler, T H (2004) GM crops: good or bad for natural enemies? In: GM crops – ecological dimensions (eds H F van Emden & A J Gray). Aspects of Applied Biology, 74, 81-90. 16. Svobodova, Z, Habustova, O, Hussein, H M, Puza, V & Sehnal, F (2012) Impact of genetically modified maize expressing Cry3Bb1 on non-target arthropods: first year results of a field study. IOBC/WPRS Bulletin, 73, 1-8. 17. Albajes, R, Lumbierres, B. Madeira, F, Comas, C et al. (2013) Field trials for assessing risks of GM maize on non-target arthropods in Europe: the Spanish experience. IOBC/WPRS Bulletin, 97,1-8. 18. Hilbeck, A, Baumgartner, M, Fried, P M. & Bigler, F (1998). Effects of transgenic Bacillus thuringiensis corn-fed prey on mortality and development time of immature Chrysoperla carnea (Neuroptera: Chrysopidae). Environmental Entomology, 27, 1-8. 19. Malone, L A, Todd, J H, Burgess, E P J & Philip, B A (2004) Will GM crops expressing insecticidal proteins harm honey bees? In: GM crops – ecological dimensions (eds H F van Emden & A J Gray). Aspects of Applied Biology, 74, 114-118 20. Hendriksma, H P, Hartel, S, Babendreier, D, Ohe, W & von der Steffan-Dewenter, I (2012) Effects of multiple Bt proteins and GNA lectin on in vitro-reared honey bee larvae. Apidologie, 43, 549-560. 21. Garcia, M, Ortego, F, Castanera, P & Farinos, G (2012) Assessment of prey-mediated effects of the coleopteran-specific toxin Cry3Bb1 on the generalist predator Atheta coriaria (Coleoptera: Staphylinidae). Bulletin of Entomological Research, 102, 293-302. 22. Birch, A N E, Geoghegan, I E, Majerus, W E N, McNicol, J W et al. (1988). Tri-trophic interactions involving pest aphids, predatory 2-spot ladybirds and transgenic potatoes expressing snowdrop lectin for aphid resistance. Molecular Breeding, 5, 75-83. 23. Alvarez-Alfageme, F, Luthi, C & Romeis, J (2012) Characterization of digestive enzymes of bruchid parasitoids-initial steps for environmental risk assessment of genetically modified legumes. PLoS ONE, 7(5), e36862. 24. Luthi, C, Alvarez-Alfageme, F & Romeis, J

(2013) Impact of alpha AI-1 expressed in genetically modified cowpea on Zabrotes subfasciatus (Coleoptera: Chrysomelidae) and its parasitoid, Dinarmus basalis (Hymenoptera: Pteromalidae). PLoS ONE, 8(6), e677857. 25. Adjei Maafo, I. K (1980) Effects of nectariless cotton trait on insect pests, parasites and predators with special reference to the effects on the reproductive characters of Heliothis spp. PhD thesis, University of Queensland, Australia. 26. Kareiva, P & Sahakian, R (1990) Tritrophic effects of a simple architectural mutation in pea plants. Nature, 345, 433-434. 27. Wickremasinghe, M G V & van Emden, H F (1992) Reactions of female parasitoids, particularly Aphidius rhopalopsiphi, to volatile chemical cues from the host plants of theiraphid prey. Physiological Entomology, 17: 291 304. 28. Gowling, G R & van Emden, H F (1994) Falling aphids enhance impact of biological control by parasitoids on partially aphid resistant plant varieties. Annals of Applied Biology, 125, 233 242. 29. Shaver, T N & Wolfenbarger, D A (1976) Gossypol: influence on toxicity of three insecticides to tobacco budworm. Environmental Entomology, 5, 192-194. 30. Yu, S J & Hsu, E L (1985) Induction of hydrolases by allelochemicals and host plants in fall armyworm (Lepidoptera: Noctuidae) larvae. Environmental Entomology, 14, 512-515. 31. Kennedy, G G (1984) 2-tridecanone, tomatoes and Heliothis zea: potential incompatibility of plant antibiosis with insecticidal control. Entomologia Experimentalis et Applicata, 35, 305-311. 32. Hariprasad, K V & van Emden, H F (2014) Effect of partial plant resistance in brassicas on tolerance of diamondback moth (Plutella xylostella) larvae to cypermethrin. International Journal of Pest Management, 60 (in press). 33. Plapp, F W Jr (1981) Ways and means of avoiding or ameliorating resistance to insecticides. Proceedings of Symposia at thr 9th International Congress of Plant Protection, Washington D.C., 1979, 1, 244-249. 34. Tilahun, D A & van Emden, H. (1997) The susceptibility of rose grain aphid (Homoptera: Aphididae) and its parasitoid (Hymenoptera: Aphidiidae) and predator (Coleoptera: Coccinellidae) to malathion on aphid susceptible and resistant wheat cultivars. Annales de la 4e ANPP Conférence Internationale sur les Ravageurs en Agriculture, Montpellier, 1997, 1137-1148. 35. van Emden, H F & Service, M W (2004) Pest and Vector Control. Cambridge, Cambridge University Press.

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GM is a valuable technology that solves many agricultural problems in breeding and generation of new traits Professor Anthony Trewavas FRS, FRSE, The Scientific Alliance Scotland, 7-9 North St David Street Edinburgh EH2 1AW trewavas@ed.ac.uk. Martin Livermore BA (Oxon), Director, The Scientific Alliance St John’s Innovation Centre, Cowley Road, Cambridge CB4 0WS martinlivermore@scientific-alliance.org Summary In the last issue of World Agriculture, Vol. 4, No. 1, Dr Helen Wallace of GeneWatch UK wrote a highly critical analysis of the role of GM crops in world agriculture (1) . By selectively quoting only critical sources, Dr Wallace constructed a misleadingly negative case against a valuable technology. In this review, we examine her case point by point. There are costs and benefits to every human activity and it is important that all are considered and form the basis of any scientific assessment. Unlike her, we conclude that appropriately approved transgenic events, while by no means a panacea to all problems of feeding a potential nine billion, can make a significant contribution towards a safe, sustainable and secure food supply over the rest of the 21st Century. Keywords Genetic modification, plant breeding, food security, agricultural policy.

Abbreviations

DNA deoxyribonucleic acid; dsRNA double-stranded RNA; Bt Bacillus thuringiensis; EFSA European Food Standards Authority; GHG Greenhouse Gas; GM genetic modification; IRRI International Rice Research Institute; LEAF Linking Environment And Farming; N Nitrogen; rDNA recombinant DNA; RNA ribonucleic acid

Glossary Cisgenesis – Altering an organism’s genome using genetic material from a closely-related species. This differs from transgenesis in that the genetic transfer could also have occurred through natural cross-breeding because the species in question are sexually compatible. Some researchers would like cisgenesis to be subject to less stringent regulation than genetic modification in which the transfer of genetic material could not happen in the wild. Cry proteins – A class of crystalline proteins expressed by the soil bacterium Bacillus thuringiensis, which are toxic to some types of insect. Embryo rescue – An in vitro seed breeding technique which allows the progeny of diverse parents, which would not normally survive, to be

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brought to maturity. F1 hybrid – The first generation of plants produced by crossing two distinct parental types. The resulting seeds often demonstrate very desirable characteristics, but fresh seed has to be produced each season, as the uniformity is lost in succeeding generations. Intragenesis – As for cisgenesis, this is a breeding technique which transfers genetic material only between closely related species. However, it differs from cisgenesis in that it allows for the use of new gene combinations created by in vitro rearrangement. Introgression – The transfer of genetic material from one species to another via hybridisation and repeated backcrossing. Landrace – A locally-adapted strain of a cultivated plant, less genetically uniform than a conventional variety.

Mycorrhizae – A symbiotic association between soil fungi and plant roots. No-till agriculture – A method of farming in which crops are drilled straight into the ground after the previous crop has been harvested, without disturbing the soil by ploughing. This reduces energy use, helps to increase soil organic matter and moisture retention and reduces erosion. Selection pressure – The response of a population of living organisms to an external negative factor. More tolerant individuals survive and pass on greater resistance (to, for example, a herbicide) to future generations. Wildlife – A common English expression covering the nondomesticated animal, bird and insect species naturally present in the environment.

the GM debate Introduction

The case made against GM crops

r Wallace’s article makes a number of specific criticisms of GM crops, which we will address individually below. These are: The limited range of GM crops currently available The reducing effectiveness of herbicide-tolerant crops, as resistance develops. The patenting of traits, preventing farmers from saving seed for replanting. Possible negative effects on human health. Cross-contamination and liability. Negative environmental impact. Lack of delivery of promised traits in the next generation of products. Loss of autonomy for farmers and consumers. But first, by way of introduction, we should appreciate that there are two main types of objection to GM crops: ideological and those arising from a pessimistic world view. To illustrate the ideological component, consider the answers given by Lord Melchett (then Executive Director of Greenpeace UK) to questions posed in a House of Lords enquiry (2): Question 101: ‘Lord Melchett, in relation to genetic modification, what do you object to and why?’ Lord Melchett, Head of Greenpeace, UK: ‘My Lord Chairman, the fundamental objection is that there are unreliable and unpredictable risks.’ Question 105: ‘How far are you prepared to carry your objections to these developments?’ Lord Melchett: ‘I am happy to answer for Greenpeace […] Greenpeace opposes all releases to the environment of genetically modified organisms.’ Question 107: ‘Your opposition to the release of GMOs _that is an absolute and definite opposition? It is not one that is dependent on further scientific research or improved procedures being developed or any satisfaction you might get with regard to the safety or otherwise in future?’ Lord Melchett: ‘It is a permanent and definite and complete opposition based on a view that there will always be major uncertainties. It is the nature of the technology, indeed it is the nature of science, that there will not be any absolute proof. No scientist would sit before your Lordships and claim that if they were a scientist at all.’ The attitude of anti-GM activists is not that this is a technology which

Figure 1. Greenpeace protestors uproot GM crops in Norfolk (from Greenpeace) (http://www.greenpeace.org.uk/media/press-releases/greenpeace-decontaminates-gm-field-lord-melchett-arrested)

holds promise but needs more development, but a flat rejection of its potential. Rather than see well-planned scientific trials take place to address concerns about human and environmental safety, they want to close down R&D and prevent products getting to market. Figure 1 shows a field trial being destroyed in a highprofile act which led to the arrest of the protestors, including Lord Melchett. Such crop-trashing has even extended more recently to fields of golden rice, developed to provide much-needed Vitamin A in the diets of the children of poor farmers in Asia (3) There is no certainty in life for anything apart from the proverbial death and taxes. So the desire for certainty for GM crops is not a realistic critique but just an attempt to block something that Greenpeace doesn’t like. There is no risk-free world, but in the estimation of risk it is contingent on those who suggest alternatives to estimate the risk of that alternative. Lord Melchett’s responses betray a deep-seated anti-science world view and an unfortunate pessimism about the human race’s creativity and adaptability. It is undoubtedly the case that no scientist will claim certainty of safety about anything, but that includes Melchett’s preferred alternative of organic farming too. In 2011 51 people died in northern Germany from eating organic produce, with thousands physiologically injured, possibly for life (4). In a form of agriculture whose main source of N is very commonly animal manure, contamination risks will always be present. Other similar cases are in the medical literature. All GM products receive detailed safety scrutiny and

there is no record of anyone dying from consuming them. GM technology has advanced well beyond the early simple traits of herbicide resistance and Bt insect resistance. Two transformation techniques, cisgenesis and intragenesis, have been used successfully to produce plants transformed with genetic material derived only from the species itself, or related species that can normally hybridise with it (5) Foreign genes are absent in these products. Furthermore, genetic transformation can now take place at a chosen defined base sequence in the genome which is opened and modifications made. A number of crops produced in this way are in field trials, have gained good public acceptance and created problems for regulators. Are they really GM crops? Does the same ideological objection still hold? The pessimism which began to flourish in the decades after World War II is encapsulated in this quote: “The battle to feed all of humanity is over. In the 1970s hundreds of millions of people will starve to death in spite of any crash programs embarked upon now. At this late date nothing can prevent a substantial increase in the world death rate ...” (6) Debilitating pessimism like this can stifle and thus impede creativity. It is fortunate that this statement by Ehrlich was ignored by Normal Borlaug (7) and the development of the Green Revolution. Figure 2 shows how grain yields have risen steadily since 1960, while the area cultivated has remained essentially the same. While attempting to predict the future is sensible, strict limitations must apply to its usefulness, particularly over the long term.

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the GM debate capable of delivering benefits which are beyond other more established breeding techniques. Like any other technology, it carries risks as well as benefits, but we cannot afford to bypass it.

The limited range of GM crops available

Figure 2. Rising world cereal yields (right axis) and total production (left axis) while total area planted remains static (left axis) (from FAO) (http://newsimg.bbc.co.uk/media/images/42730000/gif/_42730027_world_cereals_416.gif)

New technologies cannot by their nature be predicted and because the world continues to change remorselessly what the future context would be like for any supposed projection remains unknown. Stating the problem and focussing on it usually drives potential solutions and changes the future anyway. The present buzz word of the Club of Rome is sustainability. But the assumptions that underpin those sentiments along with the precautionary principle, a principle largely used by green organisations to halt progress, imply a lack of faith in future generations being able to find adequate solutions to the problems they face. Thoughts of sustainability of a particular activity should be limited to one or two generations. Beyond that, it is likely that technological advance will have made the concept irrelevant. The Green Revolution harnessed scientific plant breeding and synthetic fertilisers to allow vastly increased cereal productivity in Asia and Latin America. (8) Now, a global population of over 7 billion has more calories available per capita than half that number not much more than 40 years ago. Nearly a billion people remain chronically malnourished, but this is a function of poverty, lack of infrastructure and poor governance rather than agricultural productivity, and is outside the scope of this review. The Green Revolution is a particularly clear example of how technology can and must be used in the agricultural sector. With the world's population set to rise by a further 2 billion or more by mid-century, farmers need access to all technologies available to raise

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productivity without ploughing more virgin land. The concept of ‘sustainable intensification’ nicely encapsulates the preferred approach and is now widely used by stakeholders in the food supply chain (9). There are big gains to be made by bringing best practices to some of the lowest yielding areas of farmland, but this will not be enough by itself to guarantee food security in a world where demand for animal products and overall energy will continue to grow faster than population itself. To have the best chance of achieving this in a way which is sustainable in the long term, all available technologies must be deployed as appropriate. Today, genetic modification is the cutting edge of agronomic technology,

Nearly all the commercially available GM crops have one or both of two important agronomic traits, herbicide tolerance and insect resistance. They are also limited primarily to the major “broad-acre” crops: soy, maize, oilseed rape (canola) and cotton (10)Nevertheless, as figure 3 shows, these two key traits have led to a large and sustained year-on-year growth in the cultivation of GM crops. The main use for most of the soy is for animal feed while the maize goes to the same market but, in the USA, is also used for biofuel production. However, Dr Wallace implies that the extent of the technology’s potential is for farmers in industrialised countries to supply the animal feed and biofuels market, with there being little to offer towards global food security. This most surely is not the case. Numerous herbicideresistant crops resistant to a range of pesticides are available through conventional breeding. However the problem with all conventional breeding is the difficulty in removing unwanted traits. So it is no surprise that glyphosate-resistant GM crops have dominated use. At the levels of exposure and use, glyphosate is remarkably innocuous to human health, but good at killing weeds.

Figure 3. The evolution of the world market for GM crops (from ISAAA) (http://www.isaaa.org/resources/publications/briefs/43/pptslides/default.asp

the GM debate Extensive use of such crops has led to the much greater advantageous use of no-till agriculture. No-till farming reduces fuel consumption and not only avoids soil compaction, loss of organic matter, reductions in microbe populations and other valuable organisms like mycorrhizae and large soil invertebrates, but properly done, virtually eliminates erosion and increases wildlife populations. Most crucially, no-till reduces GHG emissions to less than one third that of organic farms and one sixth that of conventional soils. Continuous no-till needs to be managed very differently, but is clearly sustainable in all senses of the word. No-till lends itself readily to large scale mechanical management of large areas of farmland, but could only seriously develop with the easy control of weeds. Any technology is essentially neutral and it is the socio-economic environment which determines how it is used. Genetic modification emerged at a time when existing public sector breeders – for example PBI Cambridge – were being privatised, so it was inevitably the private sector which led its commercialisation. In addition, the stringent regulatory requirements encouraged by many environmentalists have made the approvals process so expensive that only major international companies have the resources to bring GM crops to market. Because of the need to see a return on their investment, they naturally used the technology to develop crop varieties which would be bought in large volumes by farmers with the resources to benefit from them. In fact, following the original introduction of Roundup Ready™ soy to American farmers by Monsanto in the mid-1990s, there was a quite rapid uptake of the same crop in South America. The development of Bt cotton has seen millions of small-scale farmers in China, India, South Africa and other developing countries also benefitting from the technology. This is not to forget golden rice, finally approaching the market after many years of development, initially in Zurich but latterly at the IRRI in the Philippines (11). Seed will be made available free to small-scale farmers, with all rights to receive patent licence fees waived by the participating companies. For a technology which has been commercial for less than two decades, that is good progress and more developments aimed at developing-country farmers can be expected, for example from projects

funded by the Gates Foundation (12). These, too, will be donated free of charge to poor farmers.

The reducing effectiveness of herbicide-tolerant crops, as resistance develops Herbicide-tolerant GM crops are essentially all engineered to resist treatment with glyphosate, an extremely useful and widely used broad-spectrum herbicide (although there are other crops resistant, for example, to glufosinate, which can be used in rotation. Similarly, pest-resistant crops express one or more cry proteins found in Bacillus thuringiensis. These crops have not introduced new crop protection agents to farming, but have allowed their use to be extended. The possibility to use broad-spectrum herbicides across fields of established crops, to control weeds without harming the crop itself, makes weed management much easier. Bt crops, on the other hand, control certain pests which attack them, without harming non-target insects. Such crops also allow maintenance of a larger population of pest predators. These traits are very valuable to farmers, as the rapid and sustained growth in the sales of both shows. However, it is a fact of life that pests develop resistance to crop protection agents over time, and GM crops are no exception. That glyphosate is so effective (and environmentally benign) means that its use is quite ubiquitous; Roundup Ready™ crops will likely have increased its use to some extent, but from an already high baseline. Inevitably, some weeds (in North and South America) have become resistant,

but this is part of the continuing cycle which requires the constant development of new herbicides to replace those which become less effective. In practice, any problem weeds can be removed using alternative herbicides or by hoeing. The practical evidence that suggests this is not a big problem for most farmers is that sales of glyphosatetolerant varieties remain high. Farmers would not pay a premium for a trait which did not continue to give them a worthwhile benefit in terms of crop management. As for pest-resistant crops, the fact that widespread resistance has not developed after a decade, or more, of exposure of insects to (for the most part) a single Bt toxin shows that the management strategy (planting a refuge of a certain percentage of nonBt plants in a field to minimise the selection pressure for Bt-tolerance) has been very effective. The trait, as commercialised, has been used to target particular major pests and was never intended to give complete protection from insect attack. The benefit of these traits to American farmers is well illustrated in figure 4, which shows how corn (maize) varieties, having both herbicide tolerance and insect resistance, have come to dominate the market over just a few years. The revolution in genomics has changed the ease with which specific pest species can be selectively controlled. Specific small sequences of RNA, derived from double-stranded RNA degradation, switch off the expression of specific genes (13). Pests that ingest a crop engineered with a specific dsRNA have specific developmental genes switched off that are specific to the organism, which then fails to mature.

Figure 4. US market share of maize seed: conventional hybrid (blue); GM Insect Resistant (IR, red); GM Herbicide Tolerant (HT, green); GM stacked IR+HT (yellow) (from Seedbuzz.com) (http://www.seedbuzz.com/knowledge-center/article/product-life-cycles-andinnovation-in-the-us-seed-corn-industry)

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the GM debate If Bt ever becomes ineffective, alternatives are already available. Dr Wallace recognises that resistance develops in conventional farming systems, but views this in a negative light, as encouraging a ‘pesticides treadmill’ whereby farmers apply larger amounts of pesticide or turn to more toxic ones. Although overall pesticide use is growing, much of this is due to the adoption of modern farming practices in the developing world. In many countries, farmers are becoming more careful about their use of agrochemicals of all types as they realise they can save money and minimise unwanted environmental impacts (for example, the greater use of precision farming in industrialised countries). Similarly, Dr Wallace sees the development of a ‘seed treadmill’ in which farmers are locked into buying inputs from off the farm rather than being self-sufficient. In fact, as long as farmers can make an informed choice and are not dragged into unnecessary debt, their farms are likely to become considerably more productive. Her argument seems to be more about the iniquities of modern farming rather than genetic modification per se, and is effectively a reformulation of the ‘conventional’ (intensive) versus ‘organic’ (extensive) debate. Organic farms almost certainly benefit from the control of pest numbers by proximity to conventional farms.

The patenting of traits, preventing farmers from saving seed for replanting Clearly, the advent of patented traits allows suppliers more control of their technology than the pre-existing (and continuing) system of plant breeders’ rights. For example, in the UK, farmers are permitted to save seed for replanting on payment of a fee to the breeder. In the case of at least the current generation of GM seeds, the farmer pays a technology fee for the transgenic trait and enters into a contract which does not permit him to save and sow seed the following season. However, even where saving seed is an option, it is not always desirable. Farmers who quite legitimately save seed one year will often buy fresh seed after a season or two, simply to guarantee freedom from disease or to take advantage of new varieties. Farmers in some developing countries

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have often not had the option of high quality seed available to them and have continued to save seeds of their own adapted varieties, or landraces, as part of a cycle of low productivity subsistence farming. As they become able to afford fertiliser, pesticides and better tools, so they will be looking to have more productive crops and would be more open to buying protected varieties (including GM). In developed countries, farmers have become used to buying seed each year as F1 hybrids have entered the market, initially for maize and latterly for oilseed rape and a wide range of vegetables. The yield advantages of these more than offset the additional expense of purchase. There is no reason why farmers in the developing world should not move more towards a similar model, where more expensive seed and other inputs are seen as being the key to more productive and profitable cultivation.

Possible negative effects on human health It is argued that ‘Controversy remains about potential unintended effects of GM foods on human health...’ In reality, a number of hypothetical concerns are raised, for some of which one-off studies of dubious value are cited as support, for example the work of Ewens and Pusztai (14). Although such stories continue to be reported from time to time, the great majority of plant scientists and toxicologists do not see any hard evidence that any tests have shown harm to be caused by GM ingredients. Recently, for example, Professor Anne Glover, chief scientific adviser to the President of the European Commission, dismissed opposition to GM crops as ‘a form of madness’ (15). The European Academies Science Advisory Council also published a report in June 2013 which supported a move to bring policy more in line with the scientific consensus on the safety and benefits of genetically modified crops (16), The great majority of dossiers submitted to EFSA, for example, are recommended for approval by the independent scientists who review them, but a number of Member States routinely fail to follow this advice and a qualified majority in favour of approval is never achieved. Concerns about the very minor changes in genomes produced by rDNA technology seem based on a matter of principle (‘unnaturalness’) rather than practical reality.

Opposition by campaigning organisations such as Greenpeace and GeneWatch is a matter of philosophy rather than science. What is still referred to as ‘conventional’ breeding produces combinations of genes which are only revealed by their patterns of expression and, in the case of non-GM techniques such as embryo rescue, results in progeny which would not be seen by natural crossing. Mutagenesis, the products of which are happily accepted by the organic movement, scrambles genomes to produce a range of undefined mutations. GM traits, on the other hand, are subject to intense scrutiny and more is known about both their genetic makeup and composition than of any other crops we grow.

Cross-contamination and liability Agricultural crop varieties inevitably get mixed to some extent, whether by cross-pollination between related species or by contamination in the supply chain. This fact is recognised by its acceptance along the food chain, subject to specific limits, usually of the order of a few percent. However, opposition to GM crops has resulted in a much more stringent regime. In the EU, food ingredients must be labelled as GM unless they are certified as having less than 0.9% content of approved transgenic material. This is achievable, but at a cost. In fact, most GM crops are used for animal feed, with only co-products – oil, protein, lecithin etc – entering the human food chain. Although animal feed must be labelled as to its GM content, there is no requirement for meat, milk or eggs to be so labelled. A problem arises if a grower or trader suffers economic loss because small amounts of transgenic material have inadvertently been mixed in. For farmers, this is a rare occurrence, as separation distances are set to minimise the risk of cross-pollination. Further down the supply chain, crosscontamination can occur, but traders have systems in place to minimise such risks (as for any segregated commodities). Risks are insured in the same way as for other bulk commodities which do not meet the customer’s specification. The contamination events which have occasionally hit the headlines have been caused by unapproved transgenic events entering the supply chain at some point.

the GM debate These have caused major recalls and resulted in seed companies paying out large sums in compensation. However, the seriousness of such incidents is due only to the strict legislation and limits which have been put in place; no harm to humans, animals or the environment has been caused by such releases. This is in stark contrast to the occasional contamination of foods by toxins or food poisoning microorganisms.

Negative environmental impact Dr Wallace’s article again raises concerns about the impact of GM crops on the environment. She cites, in particular, the UK government-sponsored Farm Scale Evaluations (17). These trials have been the only reported attempt to study the impact of farm management systems in such detail, but their conclusions apply to the particular herbicide regime used rather than how the specific tolerance was introduced into the crop variety. It was widely reported that the cultivation of herbicidetolerant crops – oilseed rape and sugar beet specifically – could reduce weed growth and leave fewer food sources and habitats for birds and other wildlife. However, this conclusion only tells part of the story. It is well known that cultivated fields are, by and large, not the best places to find wildlife, with most species being offered better habitat and more food sources at field margins and away from farmland. Any differences between ‘conventional’ management, use of herbicide-tolerant crops, or of organic management, are in any case, swamped by the differences between crops. The field trials in the UK are, however, a trivial part of an enormous amount of research on GM safety recorded by (18). These scientists constructed a compilation of 1,783 research papers published between 2002 and 2012 on crop safety. Their general conclusion is “that the scientific research conducted so far has not detected any significant hazards directly connected with GM crops”. In brief the conclusions of this enormous survey were: 1. Little to no evidence that GM crops harm native animal species. 2. The formation of hybrids between GM crops and wild relatives certainly happens. But this happens all the time with conventional crops including mutagenised crops used by organic

farmers. It is the result of growing any crop in any area with sufficiently close wild relatives where introgression can occur. The consequence may be replacement of local wild genotypes, something that of course happens anyway and is called natural selection. 3. No detrimental effect from consumption of GM crops by any animal has yet been detected. Substantial equivalence places constraints on the actual use of GM crops. They should be nearly identical in nutrient composition and in the complement of natural pesticides, for example. 4. Every publication that has examined the question of potential incorporation of GM DNA into the human, or animal, genome has rejected it as a potential problem. Humans on average consume a gram of DNA per day containing hundreds of thousands of different genes with no indication of possible transfer through evolutionary history. This is despite recent evidence which suggests that complete genes from food may be found in human blood (19). Bacteria in the soil certainly exchange genes and occasionally with plants, but again this has continued for hundreds of millions of years. Another problem cited by Dr Wallace is the potential impact of Bt toxins on non-target organisms. In fact, the only insects affected are those which begin to eat the crop and so ingest the expressed cry protein. By this means, any effect on other, more beneficial species is avoided. Finally, her paper also talks of the decline of Monarch butterflies in North America partly due to loss of agricultural milkweed (sole food for the larvae), coincident with the increased use of glyphosatetolerant maize and soy. However, most of the milkweed on which the larvae feed is outside field margins, where it is not treated with herbicide. It is also clear that Monarch populations are very sensitive to weather conditions in Mexico, where they overwinter (20). Indeed, populations of butterflies and other insects fluctuate widely and are dependent on a range of factors. Overall, there is no evidence to suggest that GM crops offer any more chance of negative impact on the environment than conventionally-bred varieties. All farming, whether extensive or intensive, itself has a major impact on the environment. No form of farming is natural since most use the plough. The nearest to natural conditions is no-till which mimics the annual growth and decay of vegetative

material as seen in all uncontrolled meadows.

Lack of delivery of promised traits in the next generation of products As with any new technology, some early forecasts for new transgenic traits have been shown to have been overoptimistic. Salt-tolerance and nitrogen-fixation are quoted as examples of the promise of GM technology not having been fulfilled….yet. But progress on both is well under way. Transgenic crops represent the present best hope for introduction of such globally-useful traits, which other breeding techniques have failed to do. Because of the complexity and cost of bringing a new GM trait to market, companies will not follow this route if simpler alternatives are available. Genetic modification is not a magic wand, but it is a tool which allows breeders much more scope to develop traits which will minimise our use of natural resources while helping to increase food security. To dismiss it because forecasts have proved unreliable is not sensible.

Alternatives to genetic modification The International Assessment of Agricultural Knowledge, Science and Technology for Development (21) is sometimes cited as a consensus view by experts on the potential for agroecological approaches to improving yields. Crop rotation, inter-cropping, improved conventional breeding and waste reduction are also given as examples of approaches which can increase food security without the supposed risks of transgenics. It is perfectly true to say that all these approaches can help. The pitifully low yields and occasional harvest failures of many subsistence farmers can be improved by even the simplest technologies. But this is not an eitheror issue: all relevant technologies can, and should, be used in the pursuit of sustainable intensification. To talk of alternatives is to create a false dichotomy. Table 1 shows the yields of rice and wheat in a number of Asian countries, with selected high-yielding country data for comparison. There are not yet any commercially cultivated GM varieties of either rice or wheat, so these large yield differences are due to

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Table 1. 2010 yield data for wheat and rice in a number of Asian countries (FAO figures)

a range of other factors, including better varieties, optimal fertilization and irrigation and modern crop protection. However, future improvements will be generated by using all available technologies, and to ignore genetic modification for doctrinaire reasons would be foolish. The difficulties presented by the membership of the IAASTD include its poor lack of balance. These were highlighted in an article in Science (22). IAASTD is viewed instead as having an underlying political agenda, largely against industrial agriculture. The document cost $12million to produce and singularly failed to recognise that the only way to save tropical rainforest and other wild land from exploitation, arising from the pressures of increased population, is for agriculture on the remaining farmland to be as efficient as it possibly can be, within the constraints of environmental maintenance, including that of wildlife. In its promotion of small farming, in its ultra conservatism, the IAASTD, in its broadest extent, represents the desire of a green and reactionary paternalist class to maintain small farmers in their present state, instead of allowing them the choice to farm in their own way and enrich themselves by uses of whatever means they see fit to use.

Assumptions We quote from a translation of a court judgement made in the Philippines on Bt aubergine trials from a case brought by Greenpeace and others. “The deliberate genetic reconstruction of the eggplant is to alter its natural order which is meant to eliminate one feeder (the borer) in order to give undue advantage to another feeder (the humans). The genetic transformation is one designed

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to make Bt aubergine toxic to its pests (the targeted organisms). In effect, Bt aubergine kills its targeted organisms. Consequently, the testing or introduction of Bt aubergine into the Philippines, by its nature and intent, is a grave and present danger to (and an assault on) the Filipinos' constitutional right to a balanced ecology because, in any book and by any yardstick, it is an ecologically imbalancing event or phenomenon. It is a wilful and deliberate tampering of a naturally ordained feed-feeder relationship in our environment. It destroys the balance of our biodiversity. Because it violates the conjunct right of our people to a balanced ecology, the whole constitutional right of our people (as legally and logically construed) is violated”. (23) Effectively this judgement states that pests have a right to destroy crops planted and needed for humans to survive. The judgement is entirely misanthropic, anti-science, but represents Greenpeace philosophy and indeed most of those that ideologically oppose GM crops. It sees the ecology of everything else as more important than its primary species, us. Those that promote organic farming, promote the waste of land and in the third world promote inevitable poverty. History has seen a progressive change replacing ideology with pragmatism, folklore with science. There will always be need for change and improvement, no method of farming is perfect, all have different problems. At present the aim must be to reduce the area of land under cultivation, but increase yield. Leaving more land to nature will be beneficial in terms of emissions and the services that organisms other than pests provide. We have already mentioned no-till, a method ideally suited to GM crops. Integrated farm

management as practised by LEAF farmers (24) seems in our eyes to present the right combination of pragmatism with the requirements of yield and care of local wild life. “Organic” will and should remain a niche agriculture for those that wish to farm or eat it. Its yields in practice are poor and its safety must remain suspect. In our view organic is not a scientific programme, but one embedded in unrealistic romanticism. Genetic modification, despite the criticisms of Dr Wallace and others, is a powerful and valuable tool which, properly applied and regulated, has the potential to make a very real contribution to a secure supply of affordable food this century.

References 1. Wallace, Helen (2013); What role for GM crops in world agriculture?; World Agriculture, Vol 4 (1), pp 45-49. 2. House of Lords (1998). House of Lords Select Committee on European Communities. 2nd Report: EC Regulation of Genetic Modification in Agriculture. 3. Science Insider (2013). Activists destroy ‘Golden Rice’ field trial. http://news.sciencemag.org/asiapacific/2013/08/a ctivists-destroy-golden-rice-field-trial 4. EFSA (2012); E Coli: Rapid response in a crisis; 11 July 2012; http://www.efsa.europa.eu/en/press/news/120711 .htm 5. Holme, I.B., Wendt, T., and Holm, P.B. (2013). Intragenesis and cisgenesis as alternatives to transgenic crop development. Plant Biotechnology Journal 11, 395-407. 6. Ehrlich, Paul R. (1968). The Population Bomb. Ballantine Books. New York. 7. Gustafson, J P, Borlaug, N E, Raven, P H; 2010. World Food Supply and Biodiversity; World Agriculture; 2010, Vol. 1 No.2, pp. 37-41. 8. Hazell, Peter (2002), Green Revolution: Curse or Blessing?; IPRI. 9. The Royal Society (2009), Reaping the benefits: Science and the sustainable intensification of global agriculture; RS Policy document 11/09. 10. ISAAA (2013); ISAAA Brief 44-2012: Global Status of Commercialised Biotech/GM crops, 2012 11. Mayer JE, Pfeiffer W, Beyer P (2008) Biofortified crops to alleviate micronutrient malnutrition. Curr Opin Plant Biol 11:166-170. 12. http://www.gatesfoundation.org/What-WeDo/Global-Development/AgriculturalDevelopment 13. Huvenne H., and Smagghe, G. (2010). Mechanisms of dsRNA uptake in insects and potential of RNAi for pest control: a review. Journal of Insect Physiology. 56, 227-235. 14. Ewen S and Pusztai A (1999), Effect of diets containing genetically modified potatoes expressing Galanthus nivalis lectin on rat small intestine; The Lancet, Volume 354, Issue 9187, Pages 1353 – 1354, 16 October 1999; doi:10.1016/S0140-6736(98)05860-7 15. http://www.scotsman.com/business/fooddrink-agriculture/madness-of-opposition-to-gmcrops-says-glover-1-3102539 16. EASAC policy report 21; Planting the future: opportunities and challenges for using crop genetic improvement for sustainable agriculture; June 2013

the GM debate 17. Squire G R, Brooks D R, Bohan D A et al (2003); On the rationale and interpretation of the Farm Scale Evaluations of genetically-modified herbicide-tolerant crops. Philos Trans R Soc Land B Biol Sci; 358 (1439); 1779-1799. 18. Nicolia, A., Manzo, A., Vereonesi, F., and Rosselini, D. (2013). An overview of the last 10 yearsof genetically engineered crop safety research. Critical Reviews of Biotechnology doi:10.3109/07388551.2013.823595.

A field of tall maize plants

19. Spisak S, Solymosi N, Ittzes P, Bodor A, Kondor D, et al. (2013) Complete Genes May Pass from Food to Human Blood. PLoS ONE 8(7): e69805.doi:10.1371/journal.pone.0069805. 20. http://www.fs.fed.us/wildflowers/pollinators/ monarchbutterfly/migration/ 21. IAASTD (2009); International assessment of agricultural knowledge, science and technology for development, synthesis report, ed B McIntyre et al.

22. Stokstad, E. (2008). Duelling visions for a hungry world. Science 319, 1474-1477. 23. Philippines court of appeal (2013). Decision on Greenpeace vs Environmental Management Bureau. http://www.greenpeace.org/seasia/ph/PageFiles/1 26313/ca-decision-doc.pdf 24. www.leafuk.org

ÂŠ PhotographyByMK â&#x20AC;&#x201C; Fotolia.com

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Response to Professor Anthony Trewavas & Martin Livermore Dr Helen Wallace, Director, GeneWatch UK, 60 Lightwood Road, Buxton, SK 17 7BB, United Kingdom helen.wallace@genewatch.org

revewas and Livermore clearly take the view that the loss of autonomy for poorer farmers associated with purchasing patented GM seeds is justified by a number of claimed benefits. However, in practice, GM farming is in crisis as resistant weeds have become widespread in response to the use of glyphosate-resistant GM crops and secondary and resistant pests are causing increasing difficulties for farmers growing insect-resistant GM crops. Despite decades of investment and research, other products have not been delivered or have failed to reach the market place, due to poor performance and technical difficulties. GM farming in the United States has not out-performed non-GM farming in Europe (Heinemann et al. 2013, Hilbeck et al. 2013). In the US, yields are falling behind and are more variable, pesticide use is higher, the number of farms is decreasing and there is greater monopoly control over inputs. The implication that US farmers grow GM through choice because it is superior is questionable as seed catalogues show that the diversity of seeds on the market in the US has reduced significantly as a result of takeovers in the industry, with many varieties only available in combination with GM traits. In addition, the capacity to innovate on farm has reduced significantly. Although Trevewas and Livermore describe GM as a “cutting edge technology”, conventional breeding, in some cases enhanced by new technologies such as market assisted selection (MAS), has in fact delivered more crop improvements much faster and more cheaply, despite a significant diversion of resources away from conventional breeding towards GM research (Goodman, 2002; Knight, 2003; Jiang, 2013). Organic and resource-conserving agriculture can improve farmers’ livelihoods, without creating dependency on patented GM seeds and associated chemicals

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(Bennett & Franzel, 2013). However, research investment in these areas is relatively limited. Over-optimism about what GM can deliver has led to significant opportunity costs as other areas of research have been neglected. The authors describe glyphosate, which is blanket sprayed on the market-leading GM crops which are tolerant to glyphosate, as “innocuous to human health” and “environmentally benign”. This claim is not consistent with evidence in the scientific literature which suggests a number of mechanisms through which glyphosate and its common commercial formulation RoundUp may damage human health (see, for example: Koller et al. 2012; Mañas et al. 2009; Paganelli et al. 2010; Romano et al. 2010; Samsel & Seneff 2013; Thongprakaisang et al. 2013). Glyphosate accumulates in glyphosateresistant GM soybeans (Bøhn et al. 2013). Regarding environmental impacts, there are particular concerns about impacts on amphibians (Relyea & Jones 2009; Wagner et al. 2013). Disturbingly, Trevewas and Livermore downplay the negative effects on wildlife of habitat loss due to blanket spraying, including impacts on iconic species such as the Monarch butterfly. Whilst it is clear that other factors (e.g. deforestation) play a role in the Monarch’s decline it is surprising to see the role of the expansion of GM herbicide-resistant crops dismissed when it is widely acknowledged in the literature (Brower et al. 2012). In addition to the negative impacts of blanket spraying GM crops with glyphosate, further milkweed habitat has been lost due to the large areas of grassland and rangeland that have been converted to biofuel crops, especially GM maize. Studies have confirmed the link between milkweed habitat loss and glyphosate-treated fields (Harzler 2010, Pleasants and Oberhauser 2013) and the negative impact on the butterflies has been modelled, providing a convincing link

between the decimation of habitat and loss of fecundity (Zalucki & Lammers 2010). Messan and Smith (2011) conclude that herbicide has a large effect and that a reduction of herbicidal spraying is needed to stabilize the monarch butterfly population. Trevewas and Livermore fail to acknowledge the seriousness of the problem of herbicide tolerant weeds (‘superweeds’) and the harm to farmers, or the problems associated with proposed responses. The spread of glyphosate-resistant weeds in the United States is causing severe weed management problems, with nearly half of US farms affected (Fraser 2013). The dramatic increase in glyphosate use that caused this would not have been possible without glyphosateresistant GM crops. The proposed response includes new GM crops tolerant to more toxic herbicides such as 2,4-D and dicamba, which will inevitably exacerbate the environmental problems associated with blanket spraying and create a new cycle of resistant weeds (Mortensen et al. 2012). Trevewas and Livermore also claim that widespread resistance has not developed to the Bt toxins expressed by insect-resistant GM crops. However, reduced efficacy of Bt crops caused by field-evolved resistance has been reported now for some populations of 5 of 13 major pest species examined, compared with resistant populations of only one pest species in 2005 (Tabashnik et al. 2013; Van den Berg et al. 2013; Jin et al. 2013). Whilst they concede that Bt crops were never intended to give complete protection against pests, Trevewas and Livermore ignore the impact on farmers of a number of documented increases in secondary pests, which can increase significantly in numbers when targeted pests decrease (e.g. Zhao et al. 2011; Tay et al. 2013). As a response to these problems, Trevewas and Livermore highlight research on the use of

the GM debate double-stranded RNA to switch off the expression of specific genes, as a new means of pest-control. However, the use of RNA interference can give rise to unintended off-target effects and its efficacy and safety is far from being established (Heinemann et al. 2013; Lundgren et al. 2013). There is no scientific consensus on the safety of GM crops (ENSSER 2013) and there are limitations to all rat feeding studies conducted on both sides of the debate (Meyer & Hilbeck 2013). There is also evidence of commercial bias in the literature (Diels et al. 2011). Even if there were no such scientific disagreements, consumers have a right to choose to avoid GM crops for health, environmental or other reasons, such as objections to the patenting of seeds. If consumer choice is to be maintained, the introduction of GM farming to a country or region adds the costs of segregation to the food supply chain, increasing costs across the board. Failure to plant what consumers demand or to effectively segregate supplies means that US farmers have lost markets due to GM farming as exports elsewhere have been reduced (EuropaBio and BIO, 2012). Whilst the industry argues that the answer is to weaken regulation, the alternative route of not planting GM food crops at all still remains open to most developing countries. For example, India and China, despite growing GM cotton, are still rightly hesitant over planting crops such as GM brinjal (aubergine) or GM rice. Food security and trade issues are a big part of the debate, as countries seek to avoid dependency on imported GM seeds and associated chemicals.

References Bennett M, Franzel S (2013) Can organic and resource-conserving agriculture improve livelihoods? A synthesis. International Journal of Agricultural Sustainability. 2013;11(3):193–215. Bøhn T, Cuhra M, Traavik T, Sanden M, Fagan J, Primicerio R (2013) Compositional differences in soybeans on the market: glyphosate accumulates in Roundup Ready GM soybeans. Food Chemistry. doi:10.1016/j.foodchem.2013.12.054. Brower LP, Taylor OR, Williams EH, Slayback DA, Zubieta RR, Ramírez MI (2012) Decline of monarch butterflies overwintering in Mexico: is the migratory phenomenon at risk? Insect Conservation and Diversity 5(2):95–100.

Catangui MA, Berg RK (2006) Western Bean Cutworm, Striacosta albicosta (Smith) (Lepidoptera: Noctuidae), as a Potential Pest of Transgenic Cry1Ab Bacillus thuringiensis Corn Hybrids in South Dakota. Environmental Entomology 35:1439–1452. Diels J, Cunha M, Manaia C, Sabugosa-Madeira B, Silva M (2011) Association of financial or professional conflict of interest to research outcomes on health risks or nutritional assessment studies of genetically modified products. Food Policy 36(2):197–203. doi:10.1016/j.foodpol.2010.11.016. ENSSER (European Network of Scientists for Social and Environmental Responsibility) Statement: No scientific consensus on GMO safety. 21st October 2013. http://www.ensser.org/increasing-publicinformation/no-scientific-consensus-on-gmosafety/ EuropaBio and BIO (2012) EU-U.S. High Level Working Group on Jobs and Growth: Response to Consultation by EuropaBio and BIO. http://ec.europa.eu/enterprise/policies/internation al/cooperating-governments/usa/jobsgrowth/files/consultation/regulation/15europabio-bio_en.pdf Fraser K (2013) Glyphosate Resistant Weeds – Intensifying. Stratus Research. 25th January 2013. http://www.stratusresearch.com/blog07.htm Goodman M (2002) New sources of germplasm: lines, transgenes and breeders. In: Memoria congresso nacional de fitogenetica. Saltillo, Coah., Mexico: Univ. Autonimo Agr. Antonio Narro. 28–41. Hartzler RG (2010) Reduction in common milkweed (Asclepias syriaca) occurrence in Iowa cropland from 1999 to 2009. Crop Protection 29(12):1542–1544. Heinemann JA, Massaro M, Coray DS, AgapitoTenfen SZ, Wen JD (2013) Sustainability and innovation in staple crop production in the US Midwest. International Journal of Agricultural Sustainability 1–18. Heinemann JA, Agapito-Tenfen SZ, Carman JA (2013b) A comparative evaluation of the regulation of GM crops or products containing dsRNA and suggested improvements to risk assessments. Environment International 55:43–55. Hilbeck A, Lebrecht T, Vogel R, Heinemann JA, Binimelis R (2013) Farmer’s choice of seeds in four EU countries under different levels of GM crop adoption. Environmental Sciences Europe 25(1):12. Jiang G-L (2013) Plant Marker-Assisted Breeding and Conventional Breeding: Challenges and Perspectives. Advances in Crop Science and Technology. 1(3):e106. Jin L, Wei Y, Zhang L, Yang Y, Tabashnik BE, Wu Y (2013) Dominant resistance to Bt cotton and minor cross-resistance to Bt toxin Cry2Ab in cotton bollworm from China. Evolutionary Applications. 6(8):1222–1235. Knight J (2003) Crop improvement: A dying breed. Nature 421(6923):568–570. doi:10.1038/421568a. Koller VJ, Furhacker M, Nersesyan A, Misik M, Eisenbauer M, Knasmueller S (2012) Cytotoxic and DNA-damaging properties of glyphosate and Roundup in human-derived buccal epithelial cells. Arch Toxicol. 86: 805-813. Lundgren JG, Duan JJ. RNAi-Based Insecticidal Crops: Potential Effects on Nontarget Species.

BioScience. 2013;63(8):657–665. Mañas F, Peralta L, Raviolo J, et al (2009) Genotoxicity of glyphosate assessed by the Comet assay and cytogenetic tests. Environ Toxicol Pharmacol. 28: 37?41. Messan K, Smith K (2011) Short and Long Range Population Dynamics of the Monarch Butterfly (Danaus plexippus). Technical report of the Mathematical and Theoretical Biology Institute. http://mtbi.asu.edu/files/MTBIpaper_ButterflyGrou p.pdf Meyer H, Hilbeck A (2013) Rat feeding studies with genetically modified maize - a comparative evaluation of applied methods and risk assessment standards. Environmental Sciences Europe 25(1):33. Paganelli A, Gnazzo V, Acosta H, López SL, Carrasco AE (2010) Glyphosate-Based Herbicides Produce Teratogenic Effects on Vertebrates by Impairing Retinoic Acid Signaling. Chem Res Toxicol. 23(10):1586–1595. Pleasants JM, Oberhauser KS (2013) Milkweed loss in agricultural fields because of herbicide use: effect on the monarch butterfly population. Insect Conservation and Diversity 6(2):135–144. Relyea RA, Jones DK (2009) The toxicity of Roundup Original Max to 13 species of larval amphibians. Environ Toxicol Chem. 28(9):2004–2008. Romano RM, Romano MA, Bernardi MM, Furtado PV, Oliveira CA (2010) Prepubertal exposure to commercial formulation of the herbicide Glyphosate alters testosterone levels and testicular morphology. Archives of Toxicology 84(4): 309317. Samsel A, Seneff S (2013) Glyphosate’s Suppression of Cytochrome P450 Enzymes and Amino Acid Biosynthesis by the Gut Microbiome: Pathways to Modern Diseases. Entropy 15(4):1416–1463. doi:10.3390/e15041416. Tabashnik BE, Brévault T, Carrière Y (2013) Insect resistance to Bt crops: lessons from the first billion acres. Nat Biotech. 31(6):510–521. Tay WT, Soria MF, Walsh T, et al. (2013) A Brave New World for an Old World Pest: Helicoverpa armigera (Lepidoptera: Noctuidae) in Brazil. PLoS One 8(11). Thongprakaisang S, Thiantanawat A, Rangkadilok N, Suriyo T, Satayavivad J (2013) Glyphosate induces human breast cancer cells growth via estrogen receptors. Food Chem Toxicol. 59:129–136. Van den Berg J, Hilbeck A, Bøhn T (2013) Pest resistance to Cry1Ab Bt maize: Field resistance, contributing factors and lessons from South Africa. Crop Protection 54:154–160. doi:10.1016/j.cropro.2013.08.010. Wagner N, Reichenbecher W, Teichmann H, Tappeser B, Lötters S. (2013) Questions concerning the potential impact of glyphosatebased herbicides on amphibians. Environmental Toxicology and Chemistry. 32(8):1688–1700. doi:10.1002/etc.2268. Zalucki MP, Lammers JH (2010) Dispersal and egg shortfall in Monarch butterflies: what happens when the matrix is cleaned up? Ecological Entomology 35(1):84–91. Zhao JH, Ho P, Azadi, H (2011) Benefits of Bt cotton counterbalanced by secondary pests? Perceptions of ecological change in China. Environ Monit Assess. 173:985–994.

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the GM debate

In defence of GM crops Professor Anthony Trewavas FRS, FRSE, The Scientific Alliance Scotland, 7-9 North St David Street, Edinburgh EH2 1AW trewavas@ed.ac.uk. Martin Livermore BA (Oxon), Director, The Scientific Alliance St John’s Innovation Centre, Cowley Road, Cambridge CB4 0WS martinlivermore@scientific-alliance.org

lsewhere in this journal (pages 6067), we make a critique of the article by Dr Helen Wallace (Wallace, 2013), in which she argues strongly that GM crops are both unnecessary and harmful in various ways. Dr Wallace has herself responded to this criticism (pages 68-69) and the editors have kindly allowed us to provide an initial reaction, on which we hope to expand in the next edition of World Agriculture. The negative picture painted by Dr Wallace does not appear to be consistent with the fact of continued steady growth in the penetration of GM crops in both industrialised and developing countries, with the area planted in developing countries now being more than half the global total. Unless farmers are being deliberately mis-sold unsuitable crop cultivars by unscrupulous merchants and are in some way prevented from sowing conventionalcultivars in subsequent years, it is hard to avoid the conclusion that the majority of farmers are getting benefits which outweigh both the higher seed cost and any negative impacts there may be. Some of her specific criticisms, which we intend to address more fully in the next edition, are addressed below: 1. ‘…GM farming is in crisis as resistant weeds have become widespread…’ Inevitably, some weeds develop resistance to particular herbicides and it is hardly surprising that this is also the case with glyphosate. There were already some resistant species prior to the widespread use of Roundup Ready™ crops – glyphosate having already become one of the most popular broad-spectrum herbicides – and further resistance will have occurred with continued use. Resistant weeds can be controlled either with alternative herbicide or by hoeing and this situation represents the reality of farming rather than a crisis. 2. Dr Wallace compares US farming

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unfavourably with Europe, but farm management practices, crops and climatic conditions are not easily comparable. She also argues that a choice to revert to non-GM seeds has been made more difficult by the consolidation of the seed industry and the lack of diversity. However, there are still plenty of non-GM cultivars available to both conventional and organic farmers and it would be normal for any supplier to be able to propagate larger quantities of particular cultivars over only a few seasons if sufficient demand existed. The reduced range of cultivars is more likely to reflect changing patterns of demand than vice versa. 3. According to the critique of our paper, ‘conventional breeding… has in fact delivered more crop improvements much faster and more cheaply’. We would not argue that non-GM techniques can produce commercial cultivars more quickly and cheaply. Partly, this is a consequence of the greater regulatory demands on transgenic cultivars and partly that only a handful of companies have the in-depth technical resources to use rDNA techniques and successfully bring transgenic cultivars to market. Nevertheless, despite the barriers, companies continue to develop GM cultivars because they simply cannot use conventional techniques to introduce the same traits. We therefore stand by our description of GM as ‘cutting edge technology’. In addition, we regard this as an extremely useful new weapon in the armoury rather than in any way being a replacement for other breeding techniques. 4. We also consider our use of the terms ‘innocuous to human health’ and ‘environmentally benign’ to describe glyphosate to be justified. This does mean it is incapable of causing harm, simply that when glyphosate is used according to instructions there is a large margin of safety. Many active ingredients of commercial herbicides have some environmental impact. A scientific risk assessment allows any

potential problems to be identified and managed. Identifying potential mechanisms for harm, or having concerns, is not the same as providing evidence or demonstrating harm in the environment. 5. The issue of habitat loss for the Monarch butterfly and other species is not one to be taken lightly. Nevertheless, it is fair to point out that, although farmed fields are themselves relatively poor in wildlife, overall farmland management itself provides many useful habitats. It seems to us that the criticism is largely one of modern intensive farming rather than GM crops per se. The other side of the coin is that greater productivity on current arable land reduces the pressure on other natural habitats; pressure on a particular iconic species is not the same as an overall regional reduction in biodiversity. 6. We are criticised for underestimating the impact of Bt expression. As for any pesticide, some development of resistance over time is inevitable and this is simply a continuation of a struggle between farming and pests, which is effectively an ‘arms race’. The situation is analogous to the use of antibiotics, which have been of enormous benefit but whose efficacy is now suffering from widespread microbial resistance. The answer is to develop new solutions rather than decry the negative impacts of existing ones. Similarly, the criticism is levelled that secondary pests have become more of a problem with the reduction in numbers of the target species. Again, this is an expected problem and illustrates that no single control method is perfect but must often be combined with others as the farmers’ needs change. 7. We take issue with the assertion that there is no scientific consensus on the safety of GM crops. In itself, this is an unscientific statement, since all we can say is that there is no additional hazard introduced by the particular GM events currently in the

the GM debate marketplace. Consumers of course have every right to choose which foods they eat, and the choice to avoid GM for ethical reasons is easily

accommodated by buying organic food. These are our first views of the criticisms and we will provide a more

reasoned response at a later date.

Reference Wallace, Helen. (2013) World Agriculture, 4, 1, 4549. What role for GM crops in world agriculture?

ÂŠ foto76 â&#x20AC;&#x201C; Fotolia.com

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economics and social

Mitigation of water logging and salinity through biodrainage: potential and practice Professor O.P.Toky1 and Dr R. Angrish2, Department of Forestry1 and Department of Botany and Plant Physiology2, CCS Haryana Agricultural University, Hisar, India Dr. O. P.Toky ICAR Emeritus Scientist, Fellow, National Academy of Agricultural Sciences Ex Dean, Postgraduate Studies CCS Haryana Agricultural University, Hisar-125004 (India) Phone (Residence): ++91-1662-243626 Fax: ++91-1662-234952 Mobile: ++91 9896173626 E-mail: optoky@gmail.com Summary Over the past hundred years, vast areas worldwide have been used for intensive agriculture following clearance by removal of deep rooted tree vegetation or by introducing irrigation in arid zones. After decades of profitable returns, many of these domains, particularly those underlain with saline aquifers and with poor natural drainage have degraded owing to water logging and salinity. Disturbed hydrological balance in the form of sustained percolation of surplus surface rain or irrigation waters to the saline water table resulted in waterlogged and saline conditions. Surface and sub-surface drainage can be an effective remedy, but has limited applications in marginal farm lands. During the last two decades, there has been awareness of the potential for biodrainage to remove surplus soil water. This is typically effected by forming a water table depression down slope of a tree plantation or discharge area that may extend up to several meters (around) beyond the plantation. This lowers the water table below the root zone of the (surrounding) crop area. Biodrainage has low establishment costs and no effluent disposal problems. Biodrainage systems have been successfully tested worldwide, including India, and a strong case for their large scale adoption can be made. The authors opine a paradigm shift in the approach of policy makers and drainage engineers in recognizing the role of trees as potent drainage modules. Sensitization of the affected farming communities to adopt locally suited biodrainage based agroforestry models is also desired. Keywords Biodrainage, salinity, water logging, water table, socio-economical, policies.

Glossary An aquifer is an underground layer of water-bearing (water saturated) area from which groundwater can be extracted using water well. Aquifers having dissolved salts are not fit for irrigation or for potable water purposes. Biodrainage is the vertical drainage of water table through evapotranspiration of strategically planted vegetation, particularly deep rooted trees. Frequent use of the term

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â&#x20AC;&#x2DC;biodrainageâ&#x20AC;&#x2122; in scientific literature has been only post 2000. Agricultural drainage is a system of open channels, subterranean pipes through which the water level on or in the soil of a cropping area is controlled. Rio summit is the United Nations Conference on Environment and Development (UNCED) held in Rio de Janeiro from 3 to 14 June, 1992. Salinity is the excessive content of salts (generally chlorides and sulphates of

sodium, calcium and magnesium) in soil- or irrigation-water. Salinity is easily measured by measuring electrical conductivity of water. A conductivity value greater than 4000 Siemens per second is harmful for most crops. Water logging of soil agriculturally is said to occur when the water table of the groundwater is too high, so that it saturates the soil in the crop root zone, resulting in prolonged anoxic conditions.

economics and social Introduction Background:

ver the past hundred years or so, countries throughout the world have introduced intensive agriculture on various pristine domains of nature, each having its own peculiar ecology. In many cases, after a few decades profits have declined and such interventions have not remained sustainable. In this paper our primary concern is the vast area of in arid and semi-arid land where deeper layers of soil had ancient stores of salts. Here agriculture-led disturbed hydrological balance has resulted in the percolation of water with a gradual rise in salinity in the crop root zone ultimately leading to development of salt pans and water logging. These changes in irrigated lowlands due to intensive agriculture has become critical so that certain areas are non-cultivable (1,2,3). It is a matter of common knowledge that an engineering drainage system is needed in such situations to maintain a check on the salinity-water table menace, but our paper deals with the non-conventional drainage system i.e. biodrainage which has caught the attention of workers throughout the world. We shall, confine our discussion mainly to the role of trees in drainage of the water from our saturated top soils of agricultural use. We shall also briefly describe the role of trees in areas where groundwater tables have declined to abnormally low depths. We shall also suggest some policies which should be adopted. Soil water use by trees and biodrainage:

Trees can transpire large amounts of water, for example, Euperua purpurea in Amazonian rainforest was estimated to transpire 1180 kg/ day of water (4). Equally noteworthy is the ecological level interaction of deep rooted trees with groundwater. Thus, as early as 1953, Wilde et al. (5) noted that tree species influence the groundwater table by acting as biological pumps. FAO (6) highlights the positive and negative effects of trees like Eucalyptus on groundwater. However, large scale scientific use of trees in ground water control seems to be of more recent origin. The concept of biological drainage or biodrainage appears to have originated in the waterlogged agricultural areas where the conventional surface and sub-surface drainage techniques were in vogue (7). Biodrainage may be defined as the vertical drainage of water through

evapo-transpiration of strategically planted vegetation, particularly deep rooted trees with the intention of lowering the water table.

Conventional drainage and biodrainage

Success and limitations of conventional drainage:

Conventionally the control of water logging and soil salinity has been obtained through civil engineering techniques such as surface drainage, horizontal sub-surface drainage and vertical drainage (8,9,10). Surface drainage excavation of open trenches is done to drain surface water and to prevent pond formation, flooding and consequent damage to the crops. In the horizontal sub-surface drainage removal of soil water below the crop root zone is done through a network open tile drains. A better option is to install a network of perforated subterranean pipes. In either case water or dissolved salts leach into the tile drains or pipes preventing both water logging and salinity. In the vertical drainage system bore wells are dug and the water is pumped out. If not saline, this water can be used for irrigation or pumped into the adjoining canals to augment flow. In semi-arid zones, where groundwater is saline, a conjunctive use helps in irrigation and prevents a gradual rise in the water table. However, these techniques, particularly horizontal sub-surface drainage, are costly to install, maintain and sustain (1,2,11). They also have the problem of effluent control. If discharged into natural drains the saline effluent pollutes the rivers downstream. If reused, even conjunctively, salts are redistributed in the agro-ecosystem and the problem of salinity increases over a period of time. Ritzema et al.(2) opined that in developing countries like India fragmented landholdings of marginal farmers are not suitable for the adoption of these techniques as compared to more developed countries, where agriculture is carried out on an industrial scale. Advantages and disadvantages of biodrainage:

Biodrainage is an ecologically attractive concept which has the merits low cost and environmental friendliness. The limitations are a requirement of land for tree plantations, slow and uncontrolled lowering of water table, limited evacuation of salts from the

system, and vulnerability of trees to highly saline conditions. Recharge and discharge zones:

In planning a biodrainage system the need for recharge and discharge zones should be clearly understood. Recharge areas are locations from where water seeps into the water table, e.g. leaky canals or tributaries and elevated areas receiving rainfall with runoff water. However, the most significant recharge areas are the agricultural fields where liberal canal irrigation is applied. The areas where biodrainage plantations are raised to offset the recharge water are known as discharge areas. On average about 10% of land in a waterlogged agricultural landscape is to be marked as a discharge area.

Biodrainage and representative problem areas Perusal of the literature shows that two unique situations exist where large scale field level biodrainage efforts have been made. These are outlined below: Clearing of deep rooted vegetation in high rainfall zones:

In Australia the pristine deep rooted tree and heath vegetation overlaid brackish water aquifers and ancient stores of salt. This was because the annual rainfall was intercepted and evapo-transpired by the native vegetation. Introduction of intensive agriculture necessitated the clearing of this tree vegetation and its replacement with shallow rooted annual crop plants. The annual water consumption by this vegetation was less than the rainfall and as result water percolated to the underlying saline groundwater table causing its gradual rise. The twin menace of salinity and water logging appeared. Now suitable development of agroforestry systems incorporating trees are expected to reduce the salinity as the water table recedes from the root zone of commercially important annual crops (13,14,15,16). This model of â&#x20AC;&#x2DC;ecosystem mimicryâ&#x20AC;&#x2122; (17) intends to obtain a plant-water use scenario that closely imitates the pre-clearing situation. The Australian system is the most exhaustively studied disturbed agro-ecosystem that unambiguously demonstrates the necessity of harmony between water use by vegetation and aquifers (Fig. 1).

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economics and social

Figure 2. Eucalypts (Eucalyptus tereticornis) biodrainage system on the boundareis in a high water table area of Rohtak district of Haryana State in north India. Paddy is the main crop during monsoon season.

Figure 3. Eucalypts (Eucalyptus tereticornis) biodrainage on the bunds in high water table area of Hisar district of Haryana in north India. Wheat is the main crop during winter.

Figure 1. Salinization of land after clearing the forests of Eucalyptus for the purpose of agriculture in Australia. Introduction of irrigation in arid and semi-arid zones:

In semi-arid north west India, the traditional rain fed agriculture was not affected by the deep underlying saline groundwater. The introduction of canal irrigation and intensive agriculture upset this balance. Gradual seepage of the liberally used irrigation water caused a rise of the saline water table so that soils became waterlogged and saline. For example, in the western zone of Haryana, average water table depth was static at about 28 m from the ground surface between the 1930s and early 1950s. Since the commissioning of the Bhakhra canal system in 1956, the water table rose to only 6m from the ground surface by 2002 (Fig. 2, 3, 4). During the past two decades nearly 50% of the area of south-west Haryana

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Figure 4. A close view of Eucalyptus tereticornis plantation on the boundaries as explained in figure 3.

has been critically waterlogged with the water table rising to <3 m of the ground surface during this time (1).The phenomenon is worldwide, but biodrainage systems are being considered and integrated with the existing agro-ecosystems for example, in China (18), India (12,19,20,21), Israel (22), Pakistan (23) and Uzbekistan (24,25).

Impact of biodrainage on depression of water table Biodrainage certainly depresses the water table immediately underneath plantations, but in an agroforestry the objective is to lower the water table to a safer depth, well below the crop root zone in the cultivated area that

surrounds the plantation (7,12). A cone of water table depression with the lowest point near the cavity of a well is known to develop as a result of pumping from the aquifer (unconfined aquifer). Further, if two wells are operating simultaneously at a suitable distance, two â&#x20AC;&#x2DC;interferingâ&#x20AC;&#x2122; cones of depression will be formed. The draw down effect of two related Eucalyptus tereticornis block plantations was similar to the combined interacting cones of depression of two pumping wells (20).

Biodrainage and soil salinity Remediation of soils waterlogged with (fresh) water is a less common phenomenon as fresh water can be readily utilized for both agricultural and non-agricultural purposes. A more threatening situation arises where water logging involves a saline aquifer or a soil profile with an ancient store of salts. In either case interaction of a biodrainage plantation with the saline waterlogged soil becomes inevitable. It is well established that physiologically most of the trees growing under saline conditions exclude salts, especially Na+ and Clwhich are excluded by the root and do not form a part of the transpiration stream. Theoretically, therefore, these may accumulate under the plantation over a period of time. This may result in a buildup of salinity in the root zone and pose a risk to the survival of the biodrainage system itself. In Australia, a 7 year old Eucalyptus plantation surrounded by an irrigated area there was a significant lowering of the water table beneath the plantation or discharge area but no accumulation of salt with respect to the outside irrigated recharge area. However, after 15 years accumulation of salts had taken place in the capillary fringe above the water table areas (14) of this plantation. Archibald et al. (26) examined the sustainability of Eucalyptus plantations on saline discharge areas and concluded that although soil salinity develops beneath the plantations, there was an excellent survival of plantations even after 20-25 years.

Biodrainage strategies Pit versus ridge planting:

Soils waterlogged up to surface or sub-surface zones are anaerobic and the conventional pit planting technique is not feasible.

economics and social

Table 1. Survival and growth of 8-year old trees in a ‘farmer’s model’ (comprising of parallel strip biodrainage plantations in north-south direction 66 m apart and with two rows of trees on each strip on about 0.5 m raised ridges) developed in an area having acute water logging at the campus of Haryana Agricultural University , Hisar, Haryana State in north western India.

On such problematic locations soil ridges raised up to 0.5 m above the surrounding soil surface is recommended (20). This aids the better establishment and subsequent growth of seedlings on waterlogged soils as it enables them to withstand anaerobic conditions produced by prolonged water logging or ponding. The ridge planting technique is being successfully practiced by Punjab and Haryana State Forest Departments in India. Since ridges are made from the field soil, they have the same salinity. Salt tolerant species are therefore, recommended. Eucalyptus, Pongamia, Casuarina, Terminalia, etc can grow while poplars and bamboos could not survive (Table 1). To avoid excess of salts accumulation due to surface evaporation, ridges can be covered with sand to discourage capillary fringe.

Block plantations:

A block of suitable trees is planted in a waterlogged area, which causes a cone of water table depression underneath the plantation. However, the extent of lowering of the groundwater table around the surrounding recharge area has been shown to vary from a radius of 40 m (15) to 730m (20). The vast differences may be attributed to the size and other characteristics of the discharge plantation block, hydraulic conductivity of the soil and cropping pattern, recharge of the surroundings. In the planning of Australian biodrainage systems the plantation discharge areas are confined to saline or degraded areas so that less arable land is lost (26).

cannot be spared for biodrainage. Here strip plantations on field boundaries are the only alternative. In many Indian states, including Haryana, the standard unit of land with field boundaries on all four sides is an acre (0.4 ha) of about 66m length in the east-west direction and 60m width in north-south direction. Therefore a ‘farmer’s model’ comprising parallel strip biodrainage plantations in a north-south direction 66 m apart and with two rows of trees on each strip raised 0.5 m are recommended (27). This agroforestry model has been successfully tested on a pilot scale around a village (Putthi) in the district of Hisar in Haryana. The model is considered as best option from the point of view of: i) technological adoption by the farming community, ii) lowering of the water table to about 1 m over a period of 5 years and iii) remuneration to the farmers as timber (27). The authors (28) compared the biodrainage potential of ten tree species planted as per this farmer’s model (Fig. 5, 6). It was revealed that about five years old trees differed significantly in their biodrainage potential in the order: Eucalyptus tereticornis clone 10 = Eucalyptus hybrid (clone of E. tereticornis x E. camaldulensis) > Eucalyptus clone–130 = Tamarix aphylla > Prosopis juliflora > Eucalyptus clone–3 > Callistemon lanceolatus = Melia azedarach > Terminalia arjuna = Pongamia pinnata. There are several pockets of land where water logging is so acute during the post-monsoon months of end-

Strip plantations

Block plantations work well, but are not feasible where land holdings are small and fragmented where land

Figure 5. Farmers model of biodrainage developed in a waterlogged area of CCS Haryana Agricultural University at Hisar, north India. Two rows of Eucalyptus tereticornis are raised on the boundareis of the field.

Figure 6. Farmers model of biodrainage developed in a waterlogged area of CCS Haryana Agricultural University at Hisar, north India. Two rows of mesquite (Prosopis juliflora) are raised on the boundareis of the field. The vertical column in the centre of four trees on a two rowed field bund is the observation well for periodic measurement of water table.

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economics and social October to December that the top soil is saturated water so that field preparation/sowing of wheat is not possible. It is on such locations that the transfer of raised field bund technology for biodrainage is adopted even by marginal farmers without much questioning.

Future scope and conclusions

Research and development

International research efforts on biodrainage have been coordinated by an International Program for Technology and Research in Irrigation and Drainage (IPTRID) of the FAO of the UN (7). In India the Indian National Committee on Irrigation and Drainage (INCID), operating under the Ministry of Water Resources (MoWR), Government of India, coordinates national level biodrainage research funding and knowledge synthesis (29). Adoption constraints:

The conduits of surface, sub-surface and vertical drainage are essentially civil engineering structures and biodrainage may be a difficult concept for civil engineers to consider. Farmers may also be wary of any negative effects tree plantations may have with their crops. This feeling emerged at a National Level Training Program comprising senior irrigation engineers, agricultural scientists and foresters facilitated by the authors (30). However, once aware of the issues these personnel could see the feasibility and advantages of integrated conventional and biodrainage. Biodrainage cannot be effective where acute and prolonged flooding, or ponding conditions, prevail. Here only surface drainage can be effective. However, where over the years a rise in the water table is a threat, properly designed biodrainage can replace or complement subsurface and vertical drainage. In future there may be increasing exploitation of trees for better groundwater hydrology, agroforestry, forestry, urban development and a green and clean environment at large. Creation of livelihood:

Widespread adoption of biodrainage is likely to depend upon use of trees with alternative uses, for example, of poplars on alluvial plains of northwestern India, have improved the income of farmers (Fig.7). This is due to the fact that a well

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Figure 7. Block plantation of poplars (Populus deltoides) in Yamunanagar district of Haryana, north India. The water table is high and the aquifer has sweet water due to a canal passing nearby. Wheat, sugarcane and fodder crops are grown in the interspaces of poplar trees.

developed marketing system is available. Eucalypts can make a similar impact on waterlogged soils as they are well adapted to waterlogged conditions. Productivity and profitability of plantations of Eucalyptus have been revolutionized with the development of genetically improved fast growing and high yielding clonal planting material. Average productivity of commercial clones is about 20-25 m3/ ha/ yr. Where World Bank aided forestry development projects existed, many States in India have adopted clonal plantations of Eucalyptus. This has been very helpful to the farmers. It is important to note that there is no self propagation of eucalypts in India. Prosopis juliflora and Prosopis pallida, are excellent biodrainers (21), which can be used for plantations on waterlogged soils. Many of the problems of Prosopis are a result of using unsuitable strains of P. juliflora. Seeds from Peruvian material assumed to be P. pallida is superior to material of P. juliflora available in India. Prosopis pods are high in sugars, carbohydrates and protein and can be used to prepare animal cakes. It fruits annually and crops evenly in an adverse climate. P. juliflora produces wood with a high calorific value of approximately 21 MJ/kg (5000 kcal/kg), so that charcoal obtained from the wood of Prosopis species is of very high quality. Ten kg of green wood will make 1-2 kg of charcoal using traditional earth kilns, in 2-4 days. Above ground biomass from different sites varies from as little as 0.5 t/ha/yr to over 39 t/ha/yr. Frequent cutting produces small branches which are ideal for cooking, so that it provides two important and integral components for rural communities in in some parts of India, especially

Figure 8. Prosopis juliflora provides firewood for rural communities in some parts of central India. The illustration shows firewood transport along the Chambal River, about 80 km South East of Agra. This plant has been used to stabilize the sandy soils along the river and wood is transported across the river, creating a local industry. (Photo courtesy Mrs Penny Cook)

Chambal Valley (Fig. 8 shows transport of Prosopis juliflora near the Chambal River). P. juliflora has immense potential on water logged soils and promises to boost the economy of poor rural people It is grown to reduce erosion in hilly areas with unstable soils prone to high run-off. Casuarina in coastal belts and bamboos in high rainfall areas, are other very important industrial species that can be used for waterlogged conditions. In order to boost the economy of farmers, there needs to be close collaboration with the companies processing and marketing the timber. Environmental concerns:

Trees are a valuable carbon sink. They play a vital role in nutrient cycling and of restoring soil fertility, arresting soil erosion and creating a micro-climate suitable for micro- flora and microfauna. The permanent tree cover protects soil from erosion and regulates the water balance. Further, trees and shrubs are less sensitive to fertility levels than food crops and some species help to stabilize degraded land. Socio-economic concerns:

Apart from the biological and environmental roles, trees also have a significant social, religious and cultural status. Since the Rio Summit in 1992, global environmental concerns have been acknowledged as integral components of sustainable development. Planting of trees on wastelands or agricultural lands for industrial and environmental health has been initiated particularly in developing countries.

economics and social For example, in Sri Lanka perennial crop-based farming systems supply over 50% of national timber and 80% of fuel wood needs. Climate change: The rural poor in developing countries, are most at risk of adverse effects of climate change. Biodrainage/agroforestry plantations have the potential to create synergies between efforts to mitigate climate change and efforts to help poor farmers from the adverse effects of climate change. Fuel wood: A large proportion of the fuel wood for domestic energy in rural areas is harvested from the debris of agriculture and from trees growing outside the forest especially for small landholders. It is therefore, vital to plant trees which provide quality fuel wood whenever possible. Fodder: Trees play an important role in livestock production since they provide shade, shelter and fodder. Acacia, Prosopis, Leucaena, Albizia, Bauhinia, Celtis, and Grewia are some genera of immense value. Non-wood products: Wild fruits, herbs, gums, resins, etc. are abundantly produced by improved tree based systems providing diverse products which are linked to socioeconomic aspects of society. Women’s role: In rural economies of developing nations women are more knowledgeable and skillful to handle some operations such as collecting fuel wood, lopping fodder, collecting wild fruits and other non-timber tree products. There are examples, of whole tree based systems, for example, where home gardens are maintained by the women. The tools required, matching their strength need to be developed, and some training to this group can enhance the profit of the family.

Policies For the effective adoption of biodrainage agroforestry in the farming community particularly in developing countries the following policy points should serve as guide lines: To detect the places where waterlogging is expected, or has already been revealed and to identify the affected farming community. Organize trainings for rural communities that are required to achieve the goal. Promote local-level processing and marketing of timber and non-timber tree products relevant to the scale of their production. Integrated development plans

should include agroforestry/ biodrainage plantations for wood based industries and should promote market demand for farm grown timber. Strengthening of farmer groups technically and making available superior tree planting stock for the farmers. Incentives should be provided to farmers growing plantations as trees afford carbon sequestration. Site specific R&D is required. Knowledge-based adaptive plans should be prepared as per the guidelines of World Agroforestry Centre and National Organizations/Institutions.

References 1. Kumar, R (2004) Groundwater status and management strategies in Haryana. In: Groundwater use in North-west India. (ed., I P Abrol, B R Sharma & G S Sekhon), Centre for Advancement of Sustainable Agriculture, New Delhi, pp 16-26. 2. Quershi, A S, McCornick, P G, Qadir, M & Aslam, Z (2008) Managing salinity and waterlogging in the Indus Basin of Pakistan. Agricultural Water Management, 95, 1-10. 3. Aleksandrova, M, Lamers, P A, Martius, C & Tischbein B (2014) Rural vulnerability to environmental change in the irrigated lowlands of Central Asia and options for policy makers: A review. Environmental Science and Policy (in press). 4. Jordan, C F & Kline, J K (1977) Transpiration of trees in a tropical rain forest. Journal of Applied Ecology, 14, 853-60. 5. Wilde, S A, Steinbrenner R S, Pierce, R S, Dozen, R C & Pronin, D T (1953) Influence of forest cover on the state of groundwater table. Proceedings Soil Science Society of America, 17, 65-7. 6. Poore, M E D & Fries C (1985) The ecological effects of Eucalypts. Rome, Food and Agriculture Organization of the United Nations, Forestry paper No. 59, pp 1- 97. 7. Heuperman, A F, Kapoor, A S & Denecke, H W (2002) Biodrainage – Principles, Experiences and Applications. Knowledge Synthesis Report No. 6. International Programme for Technology and Research in Irrigation and Drainage (IPTRID), IPTRID Secretariat, Rome, Food and Agriculture Organization of the United Nations, pp 1-79. 8. Tanji, K K (1996) Agricultural salinity assessment and management, New York, American Society of Civil Engineers, 1996, ISBN 9 78 078 4473634. 9. Garg, B K & Gupta, I C (1997) Saline wastelands environment and plant growth, Jodhpur, Scientific Publishers,1997, ISBN 9 78 817 2331584. 10. Ritzema, H P, Satyanarayana, T V, Raman, S and Boonstra, J. (2008) Subsurface drainage to combat waterlogging and salinity in irrigated lands in India: Lessons learned in farmer’s fields. Agricultural Water Management, 95, 179-89. 11. Rao, K V G K, Sharma, S K & Kumbhare, P S (2005) Drainage requirements of alluvial soils of Haryana. In: Reclamation and Management of Waterlogged Saline Soils, (ed., K V G K Rao, M C Agarwal, O P Singh & R J Oosterbaan), Central Soil Salinity Research Institute, Karnal and CCS Haryana Agricultural University, Hisar, pp 36-49. 12. Kapoor, A S (2001) Biodrainage – A biological option for controlling waterlogging and salinity. New Delhi, Tata McGraw-Hill Publishing Co. Ltd. 2001, ISBN 9 78 007 0402317. 13. Heuperman, A F (1995) Salt and water dynamics beneath a tree plantation growing on a shallow water table. Internal Report Department of

Agriculture, Energy and Minerals, Victoria, Tatura Centre, Institute of Sustainable Irrigated Agriculture. 14. Lafroy, E C & Stirzaker, R J (1999) Agroforestry for water management in the cropping zone of southern Australia. Agroforestry Systems, 45, 277-302. 15. RIRDC (1999) The ways trees use water. Water and salinity issues in Agroforestry No. 5, Publication No. 99/37, Wembley, Rural Industries Research and Development Corporation (RIRDC), pp 1-78. 16. Crosbie, R S, Wilson B, Hughes, J D, McCulloch, C & King, W M (2008) A comparison of the water use of tree belts and pasture in recharge and discharge zones in a saline catchment in the central west of NSW, Australia. Agricultural Water Management, 95, 211-23. 17. Hatton, T J & Nulsen, R A (1999) Towards achieving functional ecosystem mimicry with respect to water cycling to southern Australian agriculture. Agroforestry Systems, 45, 1-3. 18. Zhao, C, Wang, Y, Song, Y & Li, B ( 2004) Biological drainage characteristics of alkalized desert soils in north-western China. Journal of Arid Environments, 56, 1-9. 19. Angrish, R , Toky, O P & Datta, K S ( 2006) Biological water management: Biodrainage. Current Science, 90: 897. 20. Ram, J, Garg, V K, Toky, O P, Minhas, P S, Tomar, O S, Dagar, J C & Kamra, S K (2007) Biodrainage potential of Eucalyptus tereticornis for reclamation of shallow water table areas in northwest India. Agroforestry Systems, 69, 147-65. 21. Toky, O P, Angrish, R, Datta, K S, Arora, V, Rani, C, Vasudevan, P & Harris, P J C (2011) Biodrainage for preventing waterlogging and concomitant wood yields in arid agro-ecosystems in North-Western India. Journal of Scientific and Industrial Research, 70: 639-644. 22. Gafni, A & Zohar, Y (2001) Sodicity, conventional drainage and biodrainage in Isreal. Australian Journal of Soil Research, 39, 1269-78. 23. Chaudhary, M R, Chaudhary, M A & Subhani, K M (2000) Biological control of waterlogging and impact on soil and environment. In: Proceedings Eighth ICID International Drainage Workshop, New Delhi. Vol. II,pp 209-22. 24. Khamzina, A, Lamers, J P A, Martius, C, Worbes, M & Vlek, P L G (2006) Potential of nine multipurpose tree species to reduce saline groundwater tables in the lower Amu Darya River region of Uzbekistan. Agroforestery Systems, 68, 151-56. 25. Khamzina, A. Lamers, J P A, Worbes, M, Botman, E, & Vlek, P L G (2006) Assessing the potential of trees for afforestation of degraded landscapes in the Aral Sea Basin of Uzbekistan. Agroforestry Systems, 66, 129-41. 26. Archibald, R D, Harper, R J, Fox, J E D & Silberstein, R P. (2006) Tree performance and root zone salt accumulation in three dry land Australian plantations. Agroforestry Systems, 66, 191-204. 27. Ram, J (2009) Biodrainage potential of Eucalyptus for the reclamation of water logged areas. Ph D. Thesis, Nanital India, Kumaon University. 28. Rani, C. Toky, O P, Datta, K S, Kumar, M, Arora, V, Madaan, S, Sharma, P K. & Angrish, R (2010) Physiological behaviour vis-à-vis waterlogging conditions in some tree species. Indian Journal of Plant Physiology, 15, 44-53. 29. Anon 2003. Biodrainage: status in India and other countries. New Delhi, Indian National Committee on Irrigation and Drainage (INCID), pp 1-47. 30. Angrish, R, Toky, O P & Patel, R K (2008) Biodrainage: potential and practice. National Level Training Program, Training Report. Command Area Development and Water Management (CADWM) wing, Ministry of Water Resources, Government of India, New Delhi, 1-6 February, 2008, pp 1-5.

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economics and social

Scaling Up Technology Adoption Among Poor Farmers: the Case of Seed Dr Sara Boettiger University of California, Berkeley Syngenta Foundation for Sustainable Agriculture sdb@berkeley.edu

Summary Agricultural development programmes have a long history of working toward the adoption of improved crop cultivars among poor farmers. The potential food security impacts of adopting improved cultivars are well documented and critical advances have been delivered by public plant breeding research over the decades. Adoption rates, however, still remain low and there is increasing interest in understanding why so few improved cultivars have been adopted at scale, by large numbers of farmers. The international development community has begun to explore these issues of scaling up in greater depth, considering how to successfully expand policies, programmes, or projects to impact many more people. This paper contributes to a growing literature that builds on scholarship in technology adoption theory but focuses particularly on how to scale up technology adoption, moving from hundreds of farmers to reach millions. The paper presents a simple framework for analyzing the wide range of challenges inherent in scaling up the adoption of a product or service among low-income communities in developing and emerging market countries. The potential use of the framework is illustrated with a discussion of the challenges present in seed systems when seeking to scale the adoption of improved cultivars.

Glossary Bottom of the Pyramid: socio-econom-

ic description of the 4-5 billion people who live primarily in developing and emerging market countries and who are “unserved or underserved by the large organized private sector (1).” The term also defines the field of business strategy focusing on reaching this population as a market for products and services. Bottom of the Pyramid is mostly associated with the work of C K Prahalad and Stuart Hart (2).

1. Introduction

gricultural development programmes have a long history of working toward the widespread adoption of improved crop cultivars among poor farmers in developing and emerging market countries. Empirical evidence finds that the adoption of improved cultivars significantly impacts a wide range of household poverty indicators. Particularly in staple crops, many studies have examined the relationship between poverty reduction and the use of improved cultivars (4, 5). Promoting the adoption of high-yielding cultivars, as well as those with traits conferring resistance to abiotic and biotic stresses, remains a

Cultivar: form of a plant species or crop plant in cultivation (excluding naturally occurring varieties) which needs to be propagated either by seed or vegetatively. The word 'variety' is sometimes used to describe these forms, particularly in the technology adoption literature where there terms like ‘modern variety’ and ‘high-yielding variety’ are widely used. Impact investing: practice of investing in companies, NGOs, programs, projects, and funds with the explicit inten-

tion of generating both financial returns on the investment as well as social and environmental impacts. Shared value: business concept describing how a company’s strategy to address social and environmental problems can simultaneously add value to the company. The shared value framework identifies opportunities for companies, civil society organizations, and governments to employ of marketbased competition to address social and environmental issues (3).

central goal for agricultural development policies, programmes and projects. Despite demonstrated benefits and decades of innovative plant breeding to create cultivars that serve the needs of the poor, those cultivars that have achieved widespread adoption are few and far between. The most well-known successes are the wheat and rice cultivars of the Green Revolution. More recently, the Pan African Bean Research Alliance (PABRA) has reached 18.3 million households in a decade with good quality bean seed (6)1. In Bangladesh and India the flood tolerance gene (SUB1A) has been introduced into a range of ‘mega-rice’ cultivars and there is good reason to expect scaling up (7). Maize, more than other crops, often

exhibits higher adoption rates and Thailand’s Suwan-1 is an excellent example of widespread adoption (8). In some African countries, adoption of modern maize cultivars has soared. In Kenya an estimated 70% of land under maize is planted to improved cultivars (9). There are many more technology adoption success stories that have not been documented, but there are also many failures where improved cultivars have not been adopted as broadly as we hoped, or there has been low adoption, particularly in food insecure regions, where modern cultivars are most needed. After decades of innovative plant breeding and efforts by extension services to get better seed to poor farmers, the lack of adoption is disconcerting.

1. Discussion of ‘improved cultivars’ or ‘improved varieties’ implicitly limit the discussion to improvements in genetics and not seed quality. In fact, improvements in seed quality, particularly for open pollinated varieties (OPVs), may have larger impacts on successful scaling of adoption. Seed quality is discussed in several sections of the paper, but is acknowledged here as an essential component of strategies for scaling up the adoption of improved cultivars.

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economics and social

Figure 1. Percent of Land Under Maize and Rice Planted With Improved Cultivars.

2010 World Bank data in Tanzania showed less than 17% of farming households were using improved seeds (10). Among a surveyed set of sorghum farmers in Eastern Ethiopia, only 8% of land was planted to modern cultivars (11). In Cambodia, modern rice cultivars were planted on 41% of rice-growing land, but adoption was concentrated in regions where hydrological conditions were more favorable (12). Figure 1 shows 2012-2013 figures for the percentage of maize and wheat land planted under improved cultivars across a range of sub-Saharan African countries (13).2 Despite poor adoption figures, significant public resources continue to be invested in research to improve crops for the global poor, through organisations like the CGIAR Consortium (for which the annual budget reached $1 billion in 2013) (14). The large number of cultivars produced by the research system that do not achieve widespread adoption can be seen as an indicator of missed opportunities for increasing the effectiveness of public investments directed to food security and poverty reduction.., For example 41% of the maize area Ghana was planted under one old and popular open-pollinated cultivar, Obatanpa. A further 10% was planted under cultivars released before Obatanpa (i.e. before 1992) and only 1% of maizegrowing land was planted to the many improved cultivars released since the early 1990s (15). Evidence of the lack of widespread adoption demands better investigation into the mechanisms not just of technology adoption among the poor, but in the scaling up of adoption.

Defining Successful Scaling

To explore the issues of scaling up the adoption of new cultivars it would be useful to define specifically what constitutes success. Should we, for instance, view the Ghanaian Obatanpa maize cultivar as a success? One out of twenty-seven improved cultivars released since the 1960s took twenty years to reach 41% of the land area (16). Who is to say, however, that this success rate, return on investment and time frame are not reasonable, given the context in which the uptake was achieved? This paper argues for the need to develop a more precise definition of scaling up. A good definition, however, must be built on a broader foundation of evidence than currently exists. Once we have documentation and analysis of a greater number of examples of scale in recent history, we can begin to understand successful scaling and the factors that contribute to it. The term ‘scale’ will always be used by the international development community as a general way of referencing ‘significant growth.’ For example, a working World Bank definition of scaling up cited in Hartmann and Linn (17) reads: “Scaling up means expanding, adapting and sustaining successful policies, programmes, or projects in different places and over time to reach a greater number of people.” This definition has many merits. For instance, it notes that successful scaling will require not just expansion, but also the means to adapt polices, programmes and projects. It also limits scale to that which is sustainable over time. Many examples exist of supplydriven expansion of technology adoption, where public resources have

been spent on design, development, manufacturing and distribution of product only to see the use of the product plummet once the public sector steps back. Sustainable scale implies a more demand-driven scaling that not only will reach a greater number of people but will also deliver value to them. These are important distinctions that distinguish the new literature on scaling up adoption from the old technology adoption and extension services literature. Underneath the umbrella of this broad definition, however, we need critical analysis of what scale means in the adoption of technologies among the poor, and then with even more specificity, what defines successful scaling in an individual class of technologies. This paper illustrates the importance of defining and analyzing scale differently for different classes of technologies by examining scaling up the seed of improved cultivars.

2. Diagnosing Failures to Scale In addition to a rich body of literature in economics and international development on technology adoption, new explorations of scaling up rely heavily on business literature. Much has been written on the intersection between social impact and the commercial potential within lowincome developing country markets. From CK Prahalad’s enthusiastic endorsement of opportunities at the ‘bottom of the pyramid’ (18) we have come to more nuanced views of the role of the private sector in poverty reduction (19). At the same time, in the last decade, we have seen the rise of impact investing (20), the exponential growth of multinationals based in emerging market economies (21), and broad interest in Porter and Kramer’s ‘shared value’ model (22). These and other trends have produced a wealth of scholarship about market-driven solutions in international development, some of which discuss key issues related to scaling up the adoption of agricultural technologies. Common business models for reaching rural markets have been explored (23), for example, and the discipline of rural marketing is coming into its own, particularly based on experience in India, but with broader applications for the international development field (24).

2. In presenting cultivar adoption data, it is important to note that these data are difficult to collect and often differ considerably across sources. For example, in Ghana (15) 61% of maize land was planted to improved cultivars, considerably more than the 19% estimate in Figure 1 derived from national government data during a similar period.

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economics and social A practical understanding of how to scale technology adoption demands, however, that we move beyond common business models and marketing strategies. The contributions from business are invaluable, but they must be combined with rigorous empirical knowledge of technology adoption, extension models, and development economics. Additionally, progress in learning how to scale the adoption of technologies among the poor will require disaggregation; we will need to consider specific individual classes of technologies. Scaling the use of vaccines, for instance, requires entirely different strategies to scaling the adoption of irrigation pumps. Paying attention to these differences can critically inform potential opportunities for the international development community in their efforts to catalyze scale. In addition to considering classes of technologies, it is useful to disaggregate further by dividing scaling issues into three main categories. These categories are derived from technology adoption theory and are sometimes used to diagnose why adoption failed. Examining scaling issues for a product or service requires examination of the technology across these three categories. In order to illustrate how such a simple matrix of scaling analysis can be used, this section concludes with an overview of these three categories as they relate to scaling the seed of improved cultivars.3 Then, Section 3 considers six fundamental differences in seed as a class of products and, using the scaling analysis framework, explores implications for scaling up adoption. Category 1: Value

The product did not provide value to a large number of customers. Perhaps the greatest failure in scaling the adoption of technologies across any sub-field of international development lies in the fact that we are almost always trying to scale the wrong product. Products in international development are too often developed without attention to the customers’ needs and desires. This is as true in the development of new cultivars as it is for other products. Among the improved cultivars that are produced in public plant breeding systems, there are many documented mismatches between the value farmers assign to traits and the value plant

breeders do. Formal breeding programmes may focus on one trait (e.g. yield) rather than a balance of traits that are valuable to the farmer. A farmer’s determination of the value of new cultivar might include, for instance, a balance between yield, the stability of yield, early maturity and perhaps heat tolerance. In addition to valuing the degree to which the cultivar lends itself to local production conditions and techniques, a farmer’s valuation also depends on consumer traits that are often overlooked by plant breeding programmes (25). Adoption of sweet potato with higher vitamin A, for example, depends on the cultivar’s taste, ‘mouth-feel’, aroma, and color when fried (26). The valuation of traits among farmers is also diverse and dependent on a wide range of factors. In Uganda, for example, men valued banana cultivars that made better beer and women valued those that that had better cooking quality (27). Public plant breeding programmes have recognized and made advances in this area, but much more work is needed. Successful scaling strategies will include significantly improving the channels through which farmers’ needs can inform decision-making in public plant breeding programmes (28). Another failure in attempts to scale improved cultivars relates to the assumption that value for the farmer is limited to the seed’s genetics. In fact, the quality of the seed can be as important, or more important to a farmer. Tackling quality issues is a key to increasing adoption of all improved cultivars, but it can be especially important in attempts for open pollinated varieties (OPVs) and vegetatively propagated crops. Availability of high quality seed can make all the difference in a farmer’s decision to adopt. Category 2: Information and Knowledge

The spread of information and knowledge related to the product was insufficient. A second major category of failure in scaling the adoption of improved cultivars lies in the information and knowledge systems that run parallel to the supply chain. Where marketing, extension and education services do not reach farmers, even good cultivars will fail to be adopted. Some parts of these information and knowledge

systems relate to raising awareness among farmers about new cultivars, including demonstrations of the value of the improved cultivar. Other parts involve dissemination of knowledge that, ultimately, increases the value of the cultivar to the farmer. Performance often varies dramatically with timing of planting, fertilizer use, irrigation and other factors. The gene-environment interplay is a pillar of value creation in cropping systems, and scaling up a new cultivar depends upon how these benefits are communicated to farmers. While there is deserved focus by those working in technology adoption on both the product and underlying business model, scaling will fail without this parallel system of information and knowledge. Category 3: Access

There were problems in access to the product. The third category, where failures may occur relates to a farmer’s access to the improved cultivar. Typically, this includes failures across a wide range of issues such as distribution networks of the seed, which may not bring the product to the farmer. Dynamic market effects across both formal and informal seed systems may be poorly understood and incorrectly forecasted. The timing of the availability of the seed is sometimes wrong, as farmers often have a narrow window for planting. Problems in the supply chain may cause degradation in the seed which reduces quality. Supplies of essential complementary inputs may also fail. Credit is often seen as a complementary input and also brings issues of affordability to this category . These are examples of issues which can contribute to failure in scaling because they inhibit the customer’s access to the product.

3. Diagnosing Failures in Scaling the Adoption of Improved Cultivars This section illustrates the importance of disaggregating technologies into classes when considering scaling strategies and provides examples of how to use the diagnostic framework described in Section 2. Seed, as product, has fundamental differences in production, distribution, and adoption that set it apart from other technologies.

3. Vegetatively propagated crops, such as sweetpotato and cassava, play a central role in poverty reduction. Their scaling issues, however, are significantly different. Scaling the multiplication, transportation, extension, and marketing for vegetatively propagated crops, for instance, deserve separate analysis that lies outside the remit of this paper.

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economics and social An understanding of these differences offers critical insight for the future potential to scale up adoption of improved cultivars. In advanced markets, tools to support the seed business have developed over time to accommodate the idiosyncrasies of the seed market. From credit and insurance instruments, to intellectual property rights, to technologies facilitating transportation and storage, the seed business in developed countries benefits from enabling laws, policies, technologies and business practices tailored particularly to the industry. In developing countries, however, many of these tools are the targets of intervention by the international development community. These tools can be seen as the enablers of scale. Interventions to catalyze scale, however, cannot be generalized across products. By summarizing six important differences in the production, distribution, and adoption of seed, the intention is that this paper will remind donors, impact investors, policymakers and practitioners that scaling strategies differ radically across classes of products. In access to finance, support for technological innovation, the championing of business models, changes to the underlying policy framework and many more areas, different interventions are needed to address issues of scale in the adoption of different types of technologies. A. Production lags and uncertain demand

Unlike many products, seed production is characterized by a combination of long delays and uncertain demand. The time required for multiplying seed (from breederâ&#x20AC;&#x2122;s seed to foundation seed to marketed seed) varies from two to as many as six seasons. This production lag creates a multiplier effect for uncertainty; production problems in any one of the seasons will impact the final volume available for the market. The lag additionally highlights demand forecasting as a critical element in scaling up the production of seed. Supply decisions today are based on the forecasted demand for cultivars and quantities made several years before. Also, the production lag has implications for scaling that relate to inventory costs. Crops with long production times larger stocks of seed kept for longer so more money is tied up. Business implications for inventory

turnover ratios in the seed industry vary across crops according to bulk rates and perishability. Vegetable seed inventory, of course, is less costly to hold than potato seed inventory. For industries with low inventory turnover ratios, scaling strategies may demand interventions focused on financing needs accommodating long-term cash flow. When inventories are held over long periods of time, companies may react more strongly to changes in the cost of capital. These, among many others, are important clues for the international development community seeking to scale up the production and distribution of the seed of improved cultivars. Thoughtful application of the framework for diagnosing failures in scale described in Section 2 of this paper can provide guidance on policy development, creation of financial tools for seed industry enterprises or provision of support for better demand forecasting. B. Perishability

This is a second defining characteristic with critical implications for scaling. Businesses producing, storing, transporting and delivering perishable goods are, of course, dependent on good transportation links and cold storage facilities. Investments in infrastructure and storage technologies may have especially high returns if they reduce quality losses. Production and distribution of seed also derives high value from access to modern supply chain technology (like traceability, sensor, or packaging technologies). Scaling up strategies can also be informed by the impact perishability can have on pricing strategies for seed producers. Firstly, financing opportunities for businesses selling perishable products may differ from others. Secondly, production and distribution of perishable products may involve costs of compliance with wideranging regulations. Market dynamics in perishable goods can be affected by the implications of perishability and policies developed to support the industry. In developing countries, for instance, policies governing the export cut flowers may affect industry constraints. Seed industries that are not export-led may not benefit from similar policies, and the introduction of these types of policy changes could be a potential area for catalyzing scale. C. Counter-cyclical effect

Unlike many products, seed production

suffers from an unusual counter-cyclical effect that sometimes sends demand and supply in opposite directions (29). This occurs because producers and consumers are affected differently by the same risks. For example, in a year when maize yields are low seed production (for future sales) is reduced and farmersâ&#x20AC;&#x2122; have also produced less. Scarcity increases market prices for farmers selling their maize and they decide, based on high prices, to increase the land they plant under maize for the next season. Demand for maize seed rises at a time when supply of maize seed has fallen. Conversely, if there is a bumper harvest in a good year maize floods the market, farmers may plant less maize for the next season, lowering demand in the seed market. Those same favorable conditions leave seed producers entering the next year with a higher inventory, but lower market demand. Understanding this characteristic of seed as a product should inform interventions for scaling in several areas. High returns may come from interventions that enable seed companies to have access to technologies that improve control of their production environment, for example, or access better storage facilities. This characteristic of seed markets also has implications for the financing needs of seed producers to ensure their long-term survival and growth of their enterprises. D. Responses to disasters

A fourth characteristic of seed production and distribution relates to how governments and markets respond to disasters. Seed supply and demand are critically affected by disasters and similarly essential to the recovery. In times of disaster and insecurity (for example, when civil unrest ensues, crops are wiped out by a pest or disease, or there is a prolonged drought) farmers may use their seed as grain, using up stocks that had been saved for planting in the next season.4 In addition, disasters impact the seed market when seed is moved through non-market channels to alleviate the impacts of the disaster. How, where and over what period of time emergency seed is distributed, therefore, affect the seed markets. Scaling strategies need to recognize the dynamics of how nascent seed industries are impacted by various responses to disasters and, where possible, use this analysis to inform both emergency relief efforts as well as

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economics and social explore options for building more resilience in the seed industry. E. Information asymmetries

A fifth characteristic of seed as a product relates to information availability. It may be difficult to identify the true value of the product and therefore, for example, the seller may have more information than the buyer. In some products this is relatively easily resolved. For example, demonstration of an irrigation pump or a solar lamp resolves some elements of the information asymmetry. In other products it is much more difficult. The value of a livestock vaccine, for instance, may only be demonstrated a long time after sale of the product when a disease kills non-vaccinated animals. It may take time to demonstrate the value of the new cultivar, but it is reasonably easy so to do. This characteristic primarily informs scaling strategies in category two of the diagnostic tool presented in this paper, focusing on interventions in marketing, extension and education, but it also indicates the critical dependency between marketing (for example largescale demonstrations of new cultivars) and production. Additionally, for some products brands become all-important. Strategies for scaling production, distribution, and adoption of technologies with information asymmetries offer opportunities for innovations to improve branding (for example packaging or anticounterfeiting) and marketing strategies become paramount. F. Easily reproducible goods and informal seed systems

The last characteristic of seed considered here relates to its reproducibility. Markets for some cultivars of seed are defined by the fact that they are easily reproducible. This is not true for hybrids and some crops where viability is lost in continued multiplication. For many crops important for food security, however, seed for next year can be produced from this year’s harvest. Scaling strategies for easily reproducible goods differ fundamentally from those that are difficult to reproduce. Some policies become commercially important (such as intellectual property rights) and marketing strategies fundamentally shift.

For easily reproducible goods like non-hybrid cultivars , production, distribution and marketing decisions are based around the farmer’s decision to purchase, rather than save, seed. For many cultivars (including many OPVs), scaling the adoption of seed means understanding that the farmer’s decision to adopt includes consideration of factors beyond the relative gain brought by the genetics, including central issues of quality. For the farmer, the value that spurs adoption might be, for example, seed viability or disease resistance. For reproducible goods that are not bought each year, there are also timing issues that inform scaling strategies. Forecasting requires assessments of how many seasons farmers might save seed before purchasing new. Other issues that inform scaling strategies include branding, convenience, quality, price elasticities, aftermarket support services and planned timing for the introduction of the next generation of improved cultivars. All of these provide guidance for interventions that can scale up the adoption of the seed of improved cultivars. Perhaps the biggest implication of the replicability of seed, though, in scaling up adoption lies in the fact that scaling strategies must approach both formal and informal aspects of a seed system (30). In the ‘informal’ seed system, farmers save seed, cross it with local strains or landraces and produce it for themselves and for sale. Interventions by the international development community to scale the adoption of improved cultivars must address the seed system from an integrated perspective, understanding how new cultivars flow from formal to informal systems and how they move within the informal system.

Conclusions This paper has contributed to a growing literature on scaling up the adoption of technologies by presenting a simple framework for analysis that can be used across a wide variety of products and services to understand critical issues. Two elements of disaggregation are advised. First, potential failures can be diagnosed across three interrelated categories. Failures to scale may have occurred in the past because: [1] the product did not provide value to a large number of customers; [2] the spread of information and knowledge related to the product was insufficient

4. Authors, however, are divided on the extent to which this occurs.

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among customers; [3] there were problems in customers’ access to the product. Second, there is a need for caution in adopting generalized business models and interventions for scale that are common in the current literature on scaling. Instead, this paper has illustrated the benefits of disaggregating technologies into classes to examine tailored scaling strategies. Using the scaling diagnostic framework in this paper to examine the adoption of seed of improved cultivars as a class of products, it is possible to derive practical and actionable issues that deserve the attention of donors, impact investors, policymakers and practitioners. Seed has intrinsic characteristics that, in advanced commercial markets, have led to the development of certain policies, financial services and technologies that allow the industry to function. These same tools can provide guidance for supporting growth in less advanced seed systems, ultimately improving the capacity to deliver improved cultivars to smallholder farmers. Scaling up has been a buzzword in international development for many years, languishing in ambiguity and for the most part escaping empirical analysis. The development of more precise definitions of scale in international development is necessary before real progress can be made, but this relies on a foundation of detailed analysis of past successes and failures in scaling that does not yet exist. Priority investments can be made by the international development community both in a more rigorous understanding of scaling up adoption as well as at programme-specific levels using existing diagnostic frameworks.

References 1. Prahalad, CK (2009) The Fortune At the Bottom of the Pyramid, Revised and Updated 5th Anniversary Edition: Eradicating Poverty Through Profits. FT Press. 2. Hart, S & Prahalad, CK (2002) The Fortune At the Bottom of the Pyramid. Strategy+ Business, 26, 54-67. 3. Porter, M E & Kramer, MR (2011) Creating Shared Value. Harvard business review, 89 (1/2), 62-77. 4. Kassie, M, Shiferaw, B & Muricho, G (2011) Agricultural technology, crop income, and poverty alleviation in Uganda. World Development, 39 (10) 1784-1795. 5. Asfaw, S, Kassie, M, Simtowe, F & Lipper, L (2012) Poverty reduction effects of agricultural technology adoption: A micro-evidence from rural Tanzania. Journal of Development Studies, 48 (9) 1288-1305.

economics and social 6. Sperling, L, Buruchara, R, Rubyogog, JC, Boettiger, S (2013) Getting New Varieties Out to Millions: PABRA & the Power of Partnerships. AgPartnerXChange Case Study. 7. Singh, US, Dar, MH, Sudhanshu S, Zaidi, NW, Bari, MA, Mackill, DJ, Collard, BCY, Singh, VN, Singh, JP, Reddy, JN, Singh, RK, Ismail, AM (2013) Field performance, dissemination, impact and tracking of submergence tolerant (Sub1) rice varieties in South Asia. SABRAO Journal of Breeding and Genetics, 45 (1) 112-131. 8. Le Page, L, Boettiger, S (2013) Lessons for Africa’s Emerging Seed Sector from Scaling Maize in Thailand. AgPartnerXChange Case Study. 9. Mbata, J (2013) Agribusiness Indicators: Kenya. The World Bank. 10. Thapa, S (2012) Agribusiness Indicators: Tanzania. The World Bank.11. Cavatassia, R, Lipperb, L & Narlochc, U (2011) Modern variety adoption and risk management in drought prone areas: insights from the sorghum farmers of eastern Ethiopia. Agricultural Economics 42 (2011) 279–292. 12. Wang, H, Pandey, S, Verlarde, O & Hardy B, eds (2012) Patterns of Varietal Adoption and Economics of Rice Production in Asia. IRRI. 13. World Bank (forthcoming) Agribusiness Indicators: Synthesis Report for sub-Saharan Africa. 14. Stokstad, E (2014) Global research network raises $1 billion for its centers. Science 3, 343 (6166) 17. 15. Ragasa, C, Dankyi, A, Acheampong, P, Nimo Wiredu, AN, Chapo-to, A, Asamoah, M & Tripp, R

An olive farm in Andalucia, Spain

(2013) Patterns of Adoption of Improved Maize Technologies in Ghana. IFPRI Working Paper, No 36. 16. Ibid. 17. Hartmann, A & Linn, JF (2008) Scaling up: A framework and lessons for development effectiveness from literature and practice. In: Wolfensohn Center for Development at Brookings: Working Paper 5, USA, 8. 18. Prahalad, CK (2009) The Fortune At the Bottom of the Pyramid, Revised and Updated 5th Anniversary Edition: Eradicating Poverty Through Profits. FT Press. 19. Simanis, E (2012) Reality Check At the Bottom of the Pyramid. Harvard Business Review 90 (6), 120-25. 20. Goldman, P (2 December 2013) Impact Investing: Harnessing the Power of Business for Social Good. The Guardian. 21. Gaur, Ajai S, Vikas Kumar, and Deeksha Singh (2014) Institutions, Resources, and Internationalization of Emerging Economy Firms. Journal of World Business 49 (1), 12-20. 22. Porter, M E & Kramer, MR (2011) Creating Shared Value. Harvard business review, 89 (1/2), 62-77. 23. Accenture (2013) Masters of rural markets: Profitably selling to India’s rural consumers. www.accenture.com/sitecollectiondocuments accessed 22 April 2014. 24. Modi, P (2009) Rural Marketing: Its definition and development perspective. International Journal of Rural Management 5 (1) 91-104. 25. Almekinders, C J M, Louwaars, N P & de

Buijn, G H (1994) Local seed systems and their importance for an improved seed supply in developing countries. Euphytica, 78, 207-216. 26. Afuape, S O, Nwankwo, I I M, Omodamiro, R M, Echendu, T N C & Toure A (2014) Studies on some important consumer and processing traits for breeding sweet potato for varied end-uses. American Journal of Experimental Agriculture, 4 (1), 114-124. 27. Edmeades, S, Smale, M, Renkow, M & Phaneuf, D (2004) EPTD discussion paper no. 125: Variety demand within the framework of an agricultural household model with attributes: The case of bananas in Uganda. Environment and Protection Technology Division, International Food Policy Research Institute, USA. 28. Boettiger, S & Anthony V (2013) Planning for scale brief #2: Scaling demand. Ag Partner XChange: http://media.wix.com/ugd/ ad2c36_f53dd2f8d7e9472e88235 ebd160c1b80.pdf accessed 22 April 2014. 29. Louwaars N.P. & De Boef W.S. 2012. Integrated Seed Sector Development in Africa: a Conceptual Framework for Creating Coherence Between Practices, Programs, and Policies. Journal of Crop Improvement 26: 39-59. 30. Sperling, L, Boettiger, S & Barker, I (2013) Planning for scale brief #3: Integrating seed systems. Ag Partner Xchange: http://media.wix.com/ugd/ ad2c36_b4d1abdff9894 33092daa54a6e0fbd06.pdf accessed 22 April 2014.

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economics and social

Problems of ‘Scaling up’ new crop cultivars: thoughts of an agricultural economist on wider issues in this interconnected world Professor Sir John Marsh

his paper deals with a critical issue in the uptake of technology in the developing world. New technologies are essential to ensure the increased production and reduced environmental impact agriculture needs to achieve. Initiation of a new technology often arises from the recognition of changes in an area wholly unrelated to the problems of a specific industry – for example the uptake of IT in farming, marketing and monitoring outcomes. A current example is the wish of some UK farmers to use drones to improve the precision of pesticide or fertiliser application. Crop development provides a classical example. We have ‘new’ means of generating new cultivars. They are applicable to secure a diversity of purposes such as pest resistance, drought tolerance, palatability and storage requirements. In all these areas the final test of success is at the point of consumption

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- will the amount bought at the prices that exist reward the effort involved in development. For seed the gap between the initial decision to seek a new cultivar and its use is extended in terms of time and the number of other business decisions that have to take place concurrently if the new material is to succeed. For example, the ability of a Supermarket chain to capitalise on the baseless fears of consumers about a new technology may render all the previous investment valueless. The thrust of Dr Boettiger’s paper is that publicly funded institutions get it wrong and that although successful in generating new cultivars these do not penetrate the market on a scale that justifies the resources committed. There is an additional element, in that success is judged not simply in aggregates but in terms of its distributional effect – does it serve the needs of the poor? It may be that this is an example of where the development community

puts the cart in front of the horse. Using a model that is over simple but compelling, poverty results from insufficient demand for labour. Thus, where labour supply is greater than the amount that can be profitably employed people remain without work and depend on entitlements enjoyed either as members of families and local communities or through organised social services. In reality, an activity that raises real income anywhere in an economy creates demand for more goods and services and indirectly for the labour that produces them. If improved crops make agriculture more efficient, its income will rise and secondary streams of demand will emerge. This may come about even if the new methods are only directly applicable to the competitiveness of relatively rich farmers or businesses. Thus focussing on technologies that are directly applicable to the poor may be misguided.

economics and social

Smart Metrics and Data Management Strategies for Public Private Partnerships Dr Sara Boettiger University of California, Berkeley Syngenta Foundation for Sustainable Agriculture Glossary Impact investing: The practice of

investing in companies, NGOs, programs, projects, and funds with the explicit intention of generating both financial returns on the investment as well as social and environmental impacts. Private sector: For the purpose of this paper, the private sector consists of organizations with private interest goals (for-profit) rather than public interest goals. It is recognized that the lines between public and private sectors are not definitive. There are, for

Introduction

ollaborations across public and private sectors are needed to address the challenges facing our planet. Increasingly, we are turning to publicprivate partnerships (PPPs) to create social and environmental changes. Today’s PPPs, though, are far removed from those of past decades where governments and companies would partner to build infrastructure or provide public services. In agricultural development, PPPs are found throughout the value chain, from input supply through to the sustainable sourcing of commodities from smallholder farmers. PPPs in telecommunications, banking, and IT are also changing the lives of poor farmers around the world. These partnerships are becoming more common in agricultural development, and they are attracting larger investments. Grow Africa, for example, is a US$3.5 billion consortium of companies, public sector organizations, the World Economic Forum, and the African Union, investing in African agriculture (2). The challenges of structuring and managing PPPs in agricultural development are becoming more familiar, but some areas remain

example, many hybrid entities that have elements of both public and private interest goals. Public-private partnership (PPP): The definition of this term varies widely and there is continuing debate about what constitutes a public-private partnership. In this paper, the term is used to describe a collaboration between public and private sector entities in which partners engage in the activities of the partnership, sharing in the costs, benefits, and risks (1). A distinction is drawn between partners engaged in activities and entities whose sole purpose is

financing; the latter is not considered a partner in a PPP. An NGO’s publicinterest project with funding from a company, for example, is not considered a public-private partnership. Public sector: This paper uses the term public sector to describe an organization with a public interest mandate, including: universities, foundations, aid agencies, international organizations, NGOs and others. The term is used to distinguish the functional mandate of an organization, rather than its legal structure.

relatively unexplored. Critical gaps in our knowledge relate to the use of metrics in PPPs and strategies to manage data across the public-private interface. Questions about what you measure, how you measure it and with whom you share the data are approached very differently by companies and public sector organizations, and the compromises reached will have tremendous impact on the course of agricultural development.

for learning. Each partner has the potential to get better at the craft of structuring and managing PPPs, but those lessons can also be codified for widespread application through the measurement of successes and failures. More broadly, we also need evidence of whether PPPs really are a good way of realizing social and environmental impacts. The champions of PPPs who hail them as an efficient instrument of development thus far do not have strong evidence indicating whether PPPs really do accomplish public interest goals. Lastly, the management of data across the public-private interface is paramount to the future of agricultural development. In global business, we have entered an era where the strategic use of data is an increasingly important determinant of success (3). Companies with the tools to collect, analyze and create business opportunities from data are at a competitive advantage. The powerful new uses of data are poised to also revolutionize international development. As it becomes more common for PPPs to generate data, there is a need for strategic data management to ensure these valuable resources continue to support public interest goals. PPPs may also develop with the

Why Should We Care About Metrics in PPPs? We are all familiar with the old adage, ‘you can’t manage what you don’t measure.’ Metrics can improve public-private partnerships by creating a foundation for evidence-based decisions to make real-time changes in operations when they are needed. Metrics can improve the allocation of resources and create incentives that drive behavior in parties at all levels of the PPP. Improved management of PPPs through the use of metrics frameworks will lead to more efficient progress toward agricultural development goals. In addition to better management of PPPs, however, metrics are important

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economics and social purpose of accessing sources of data and analytical tools. We have seen this for many years already in plant genomics PPPs (4). Either way, data issues are likely to be at the core of more and more PPPs in agriculture.

Practical Difficulties in Metrics and Data Management Strategies Despite the value of good metrics and data management strategies, those who have worked to develop PPPs know how difficult it can be to reach agreement. There are many differences in how public and private partners approach metrics and the use of data in PPPs. Private partners in a PPP have concerns that affect confidentiality of the management data and what to measure. Cost concerns are different between public and private partners, as are time frames. A public sector partner may be familiar with after-thefact, expensive and in-depth monitoring and evaluation frameworks found in the academic world. Companies, on the other hand, may insist on real-time data and weigh the cost of obtaining data against the value they deliver. These are only a few examples in a panoply of differences in how public and private sectors approach measurement and data management strategies. Also, any previous commitments the partners have to measurement standards need to be accommodated. These may come directly from organizations like the Global Reporting Institute, or the Global Impact Investing Network’s IRIS or others. Donors or impact investors funding a PPP sometimes attach inflexible metrics frameworks to their investments. Previous commitments may also be rooted in a belief in the value of one type of tool, such as randomized control trials, or they may derive from partner’s historical commitment to a particular measure.

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Creating a metrics strategy in a PPP can be further hindered by a mismatch in the skills of the people engaged. Legal and management staff charged with setting up a PPP may not be the right people to craft a creative metrics and data management strategy that includes institutional commitments, heeds organizational constraints, complies with intellectual property rights policies, acknowledges capacity differences, supports partners’ goals and other factors. Bringing in expertise from outside is a possibility. The common decision made by organizations considering whether to invest in training staff or hire-in external expertise exists here. As a partner engages in more partnerships, it may become worthwhile to develop in-house expertise, but newer entrants and smaller partners will seek consultants with external expertise. Field experts in monitoring and evaluation or metrics will bring a wealth of sector-specific knowledge. They may, however, lack appreciation for the nuances of the public-private interface and, especially, be unfamiliar with newer models of dual use in data management where partners seek to commoditize data while also ‘do good’ with it.

A Role for Donors Given the challenges faced by PPPs as they try to implement smart metrics and data management strategies, donors in agricultural development have an important leadership role to play. Many governments, foundations and impact investors finance PPPs with the belief that that they are critical tools for accomplishing public interest social and environmental goals, and that PPPs provide prudent investments for scarce development funds. These claims, for the most part, have yet to be corroborated. Donors can take the lead in creating better metrics to assess the impact of PPPs in agricultural development.

The role of donors is broader, though, than their responsibility to measure the impact of PPPs. They have a vested interest in improving the quality of PPPs and supporting their success. For this, donors need to be active in promoting best practices in the aspects of metrics strategies that improve real-time operations of partnerships and create incentives within partnerships. For some donors this leadership role will be challenging, requiring the ability to step away from their more public-sector historical use of metrics and embrace the ways in which modern companies collect and use data. Other donors are more at the cutting edge of measurement issues at the public-private interface. Perhaps most importantly, donors need understand new models of data management for public-private projects. In agribusiness, as elsewhere, companies are using data in new ways and on an unprecedented scale. Without leadership from donors, public sector partners entering into PPPs may make critical mistakes in data management strategies with farreaching implications. Regardless of how they choose to take the lead, the call to action is clear. Donors have new responsibilities to support better metrics and data measurement strategies in the agricultural development PPPs they fund.

References 1. Spielman, D J, Hartwich, F & Grebmer, K (2010) Public–private Partnerships and Developing?country Agriculture: Evidence From the International Agricultural Research System. Public Administration and Development 30 (4), 26176. 2. Juma, C (2013) Development: Starved for solutions. Nature, 500, 148-149. 3. Manyika, J, Chui, M et al. (2011) Big Data: The Next Frontier for Innovation, Competition, and Productivity. McKinsey Global Institute Report. 4. Boettiger, S, Anthony, V, Booker, K, Starbuck, C (2012) Public-Private Partnerships in Plant Genomics for Global Food Security. IDRC web: http://www.idrc.ca/EN/Documents/Public-PrivatePartnerships-in-Plant-Genomics-for-Global-FoodSecurity.pdf Accessed 27 April 2014.

comments

A response to the article “What role for GM crops in world agriculture?” Letter to the Editor Sir

I was surprised to see the article “What role for GM crops in world agriculture?” in the summer 2013 edition of World Agriculture. It is good to present a range of views on important topics, even if members of the editorial board do not personally agree with them. However, Dr Wallace does little to address the potential contribution of crop biotechnology to farming in developing countries (as the summary suggests) but uses the bulk of the article to rehearse the well-worn arguments of activists about hypothetical safety issues and corporate control of the food chain. The author suggests that, because early optimistic statements about the potential of genetic modification to produce salt-tolerant and nitrogen-

fixing crops have not yet been realised, it should effectively be written off because of the greater advances made through conventional breeding. Wat she fails to realise is that there is no silver bullet offered by any one technique, and that researchers (and the funders of research) should have an open mind about the potential benefits of all available technologies. Readers will be aware of the latest work from Professor Cocking’s group at the University of Nottingham on the discovery of nitrogen-fixing bacteria which are capable of colonising all major crop plants. This is a very significant advance, but the fact that it has been achieved by non-GM means is no argument for ignoring the very real benefits biotechnology can bring when such solutions do not present

themselves. Given the major additional hurdles to be overcome to get a new transgenic event approved, companies will not continue to invest in the area if they could achieve as much in other ways. While I applaud the editorial board of WA for being willing to publish a wide range of views, I think that in this case it was not helpful to print an article which attacks the very concept of GM crops. Criticism is to be welcomed when a good case can be made, but doctrinaire opposition is another matter. Martin Livermore Scientific Alliance St John's Innovation Centre Cowley Road Cambridge CB4 OWS Tel: +44 1223 421

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