Table Of ContentARTICLE IN PRESS
CropProtection23(2004)757–781
Review
A critical assessment of organic farming-and-food assertions with
particular respect to the UK and the potential environmental benefits
of no-till agriculture
Anthony Trewavas*
ICMB,UniversityofEdinburgh,MayfieldRoad,EdinburghEH93JH,UK
Received3September2003;accepted21January2004
Abstract
Thereiscurrentlyconsiderablediscussionaboutthemeritsofparticularformsofagriculture.Thediscussionhasbeengenerated
byexcessfoodproductionintheEC,continuingpublicdisquietovertheuseofchemicalsinfoodproductionandpoliticalagitation.
Muchofthedebateconcernsthemeritsorotherwiseoforganicagriculturewhichisoftenseenbythepublicasproducingfoodfree
of chemicals and being more environmentally friendly. This article examines these notions critically dealing with each of the
individual claims frequently made for organic agriculture. The article concludes that in the UK, at least, when problems with
agriculture emerge they usually hinge around poor management not mode of agriculture. In environmental terms no-till farming
currently seems to bebetter thanothers. Thebenefits of holisticthinking byfarmersare indicated.
r2004Elsevier Ltd. Allrightsreserved.
Keywords: Organicfarming;Soiluse;No-till;Pesticides;Farmenvironment
Contents
1. Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 758
1.1. Comparisons betweendifferentkinds ofagriculture to examine strengthsand weaknesses. . . . . 759
2. Pesticide traces inconventionally produced foodcauses cancer. . . . . . . . . . . . . . . . . . . . . . 760
2.1. Background . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 760
2.2. Agricultural exposure topesticides and cancer . . . . . . . . . . . . . . . . . . . . . . . . . . . 761
2.3. Possible xeno-oestrogenic effectsof pesticides . . . . . . . . . . . . . . . . . . . . . . . . . . . 762
2.4. A diethigh infruits andvegetablescuts cancer ratesin half . . . . . . . . . . . . . . . . . . . . 762
2.5. Hormesis indicates the potential valueof synthetic chemicals in the diet. . . . . . . . . . . . . . 763
2.6. The priceof fruitandvegetablesdetermines health. . . . . . . . . . . . . . . . . . . . . . . . . 763
2.7. Conclusion onpesticides and cancer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 763
2.8. Where organicnaturalism ideology leads . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 764
3. Comparisons oforganic andconventional soil properties. . . . . . . . . . . . . . . . . . . . . . . . . 765
3.1. Is alow organicyield more natural? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 765
3.2. Why are organicyields lower? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 765
3.3. Is soilfertility better onorganicfarms?. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 766
3.4. Is organicsoil structure better? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 766
3.5. Doorganic soilshave greatermicrobial diversity? . . . . . . . . . . . . . . . . . . . . . . . . . 767
3.6. Doconventional farms pollutewaterways withnitrate andorganicfarms donot?. . . . . . . . . 767
3.7. Dosoluble minerals damagethe soil?. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 767
3.8. Is mineral recyclingonorganic farmssustainable? . . . . . . . . . . . . . . . . . . . . . . . . . 767
*Tel.:+44-131-6505328;fax:+44-131-6513331.
E-mailaddress:[email protected](A.Trewavas).
0261-2194/$-seefrontmatterr2004ElsevierLtd.Allrightsreserved.
doi:10.1016/j.cropro.2004.01.009
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3.9. Is manurebetter thanminerals?. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 768
3.10. Conclusion onorganic soils . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 769
4. Is organicfood morenutritious, healthier andtastier thanconventional products? . . . . . . . . . . . 769
5. Is organicfarming environmentally superior?. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 770
5.1. Measurements onthe samefarm . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 770
5.2. Measurements comparing different farms. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 770
5.3. Biodiversity indicesof invertebrates on organicandconventional fields . . . . . . . . . . . . . . 771
5.4. Birdpopulations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 771
5.5. Conclusion onenvironmental issues . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 772
6. Changing toorganic farming wouldlowercosts of agriculture . . . . . . . . . . . . . . . . . . . . . . 772
7. Organic uses lessoverall energy. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 773
8. Benefits to the useof GMherbicide tolerant crops—thesuperiority of no-till agriculture over
organic andconventional agriculture for the environment . . . . . . . . . . . . . . . . . . . . . . . . 774
8.1. Advantagesof no-till agriculture comparedto tilled organicandconventional fields . . . . . . . 774
8.2. Conclusions onno-till. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 775
9. Critical assessment of published organicpapers. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 775
10. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 777
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 778
References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 778
1. Introduction by DeGregori (2004). The notion of self-sufficiency was
formulated at a time when it was thought agricultural
Organic agriculture has developed rapidly in the resources were running out. However there is sufficient
European Community. An excess of food production phosphaterocktolast1000years(Simon,1996)andthe
and an increase of wealth enables different but less Haber Bosch method converting gaseous nitrogen to
efficient forms of agriculture to survive. However ammonia can provide for unlimited fertiliser N (Smil,
organic agriculture is different to other current forms 2000a). The only resource that might constrain agricul-
such as conventional agriculture or integrated farm turecouldbeavailablefarmland,butorganicagriculture
management (IFM) because it has a well-established is less efficient in its use of land. Instead of lack of
ideological base and groups of often vociferous suppor- resources,itisnowresourceover-use,theglobalimpact
ters who are usually not farmers. This situation has led of their use along with global warming and a growing
to claims about organic agriculture which is the subject population that represent major concerns (Trewavas,
of this critical article. The three primary points are; (1) 2003). Where appropriate these problems are referred
thatorganicfoodishealthierbecauseitdoesnotcontain to. A common claim, that agriculture has failed, is
synthetic pesticide traces, (2) that the soil structure on simply contradicted by the abundance of produce in
organic farms is much better leading to less pollution present day supermarkets.
from nitrate and is healthier for the crop plant, and (3) In a democratic society those who wish to farm
that environmentally organic is better than the other organically (or biodynamically) or to eat organic food
forms and is chemical free. Each of these claims is have a perfect right to do so. It would be helpful if the
examined in turn and in some detail. organic ideological community would recognise that
Organic farming owes its origins in part to the right in reverse for others to farm in the way they wish.
development of biodynamic farming by Steiner (1958). Inapluralistsocietyallhaverights.GMcropswouldbe
However this form of farming with its belief in cosmic the simplest way to introduce the enormous environ-
forces has no place in any scientific discussion and is mental benefits of no-till agriculture, but organic
considered occult in character (Kirchmann, 1994). regulations that insist that organic food must have
Organic agriculture, at least in the UK, built upon zero GM presence are in turn an attempt to impose
aspects of Steiner in terms of self-sufficiency of small organic regulations on everyone else and may limit
farms, a belief in the health of soil producing healthy the introduction of widespread no-till to UK agricul-
plants (and healthy people) and a rejection like Steiner ture. As in all industrial processes, certain tolerances
oftheuseofanychemicals(Balfour,1948).Thegeneral in production are accepted and these should be
historyoftheorganicdebatehasbeendescribedindetail instituted.
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1.1. Comparisons between different kinds of agriculture
Biocontrol Regulations
to examine strengths and weaknesses
Price
Machinery
Throughout this article comparison is made between Pesticides Land maintenance
Fertiliser
different kinds of agriculture. Organic agriculture is Wildlife
Livestock
definedbyitsregulations.IntegratedFarmManagement Farmer Yield Seed
is defined by the LEAFUK (Linking environment and Transport
Farming)audit,themainIFMgroupintheUK.LEAF Soil
Season Fields Crops
specifies exacting standards of landscape, hedgerow
Milk, meat
maintenance, large field margins, quality soils and Manure Weeds
Pests
provides good animal welfare (Drummond, 2000), all Temperature
Weather
supposedly features only of organic farms in the public
mind. But what exactly is conventional farming other
Fig. 1. A simplified view of a farm as a system. A system can be
than simply not being organic? And when comparisons regardedasanetworkcomposedofinter-linkedelementsthatinfluence
are made, what evidence is there that the conventional eachother.Aboundarycanbedrawnaroundthesystemtosimplify
farm is representative of this weakly characterised understanding. To demonstrate linkages within the system it is
sufficient to indicate that modification of one component modifies
farming procedure in any way. Unless evidence is
othersinturn.Inthefiguretheselinkagesaredrawnasdottedlines.A
provided on this point and perhaps the average
proper systems structure would attempt to estimate the strength of
conventional and average organic farm stipulated, linkages although bearing in mind that the strength will vary with
published comparisons should be treated critically. Use circumstance (for example, manure will affect crop yield less if
of best practice conventional and organic farms (if that minerals have previously been added). But in a farm all system
constituents are ultimately linked to the farmer and his ability to
can also be defined) might improve the quality of
adaptively manage. Successful farmers appreciate the systems nature
comparison. The only specific features that really
oftheirfarmandactaccordinglyalthoughtheymaydothisintuitively
distinguish organic from all other forms of farming are and with wisdom gained from experience. The context around the
a rejection of soluble minerals as fertiliser and synthetic boundaryiscomposedofweather,cropprice,pricevolatilityandother
pesticides in favour of natural ones. Any conventional financialarrangementsthatinfluencetheoverallfarmsystemstructure.
farmercanchoosetoincorporatethesupposedlyunique
organic environmental features into their farm and
many clearly do; incorporation of manure to save on In simpler terms we can recognise standards of farming
fertiliser, for example. excellence much as is commonly recognised in science,
The variety of conventional farming procedures and education and medicine. It is not difficult to recognise
farms causes difficulty in attempting comparisons. Not low farm standards; rusting machinery, half covered in
only do UK farms vary in climatic experience, ranging grass; un-maintained or no hedges; holes in barn roofs,
over nearly a 1000 miles of latitude, varying in rainfall, un-repaired gates; a pool of excrement outside the
wind, average temperatures, exposure, slope, soil types cowshed and so on. Furthermore, poor management
andquality,mixedandarable,hedgerowstructure,weed andlackofbiologicalunderstandingresultsinexcessive
and pest problems but they also vary in managerial use of costly pesticides thus wasting money; failure to
quality and attitude, level of farmer education, farmer use manure on a mixed farm to offset fertiliser costs
understanding and finally wealth. Although attempts wastes money, as well as failing to take advantage to
are made to supposedly match soil quality when maintainsoilquality;poortreatmentofanimalsleadsto
comparing conventional and organic farms, recent loweryields;failuretomaintainhedgerowsorlargefield
investigations using GPS controlled metre-by-metre margins limits pest predator numbers requiring more
surveys (precision farming) have indicated how variable pesticide and so on. When farms fail the commonest
is both the organic and mineral content of supposedly reason is apparently poor financial, that is managerial,
uniformfields(Smil,2000a).Comparisonsthataremade control in the face of a variable market (Hansen and
betweenconventionalandorganicfarmscommonlyrely Jones, 1996). The IFM and organic benefits of wide
on farms nearby to each other to minimise (but not to margins, soil quality, landscape and good animal
eliminate) environmental variation. The presence (or welfare help to limit the year-to-year variation in
absence) of trees and hedgerows which modify environ- income, the major enemy of sustainable farm practice.
mental impact are usually ignored. But managerial Perhapsthecrucialfeaturehereisthatcomparisonof
quality itself invariably fails to be investigated or well-managed and poorly managed conventional farms
estimated even though it is of obvious importance. will result in all the same landscape and animal welfare
What exactly is farm managerial quality? A farm is a differencesas those supposedly separating organic from
densely interlinked structure forming a system or net- conventional. The answer to this difficulty in scientific
work that isultimately controlled bythe farmer and his comparison of organic and conventional farming is
degree of understanding of its behaviour (Fig. 1). simply to emphasise comparisons made on the same
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farm,matchedfieldsandusingthesamefarmertoavoid potential recruits were rejected for army service in the
managerial variation in standard. Boer war because of poor stature and weight resulting
Mostorganicfarmsaresupposedtoremainsmalland frompoordiet(DrummondandWilbraham,1940;Orr,
self-sufficientwhereasconventionalfarmsareincreasing 1936). Price and the knock on effects on consumption
in size the result of economic pressures. It will be are major concerns with organic food and one which
increasinglydifficulttomakevalidcomparisonsbetween should not be ignored. Food abundance reduces price.
thetwo.Farms,ofnecessity,dointeractwitheachother
andotherfacetsofthecommercialandfoodproduction
community, constructing a complicated network. From 2. Pesticidetracesinconventionallyproducedfoodcauses
what we now understand about network stability, small cancer
farms interacting minimally as a result of a policy of
self-sufficiency do not generate stable networks, which 2.1. Background
instead require a limited number of hubs with very
numerous interactive links (such as large conventional Chemophobia, the unreasonable fear of chemicals, is
farms) coupled to many smaller constituents with fewer a common public reaction to scientific or media reports
links (Barabasi, 2002). Organic regulations if expressed suggesting that exposure to various environmental
country-wide run directly counter to efforts to stabilise contaminants may pose a threat to health (Safe, 1995).
agricultural production. One possible structure that The spectre of cancer birth defects and irreversible
mightbemorestableisadiversemulti-hubnetworkbut effects invariably scares people and various groups that
this would see organic agriculture as merely a niche campaign on environmental issues find the anxiety
activity, not a primary form of agriculture. raised a useful source of political issue. Virtually all
Poor management survives because of subsidies, the chemicals can be shown to be dangerous at high doses
curse of quality farming practice. Will organic action and this includes the thousands of natural chemicals
plans upgrade managerial standards then? Organic that are consumed every day in food but most
farming is recognised as higher risk (Leake, 1997) particularly in fruit and vegetables.
becauseofcropfailureandmarketvariation.Thusonly The assessment of chemical safety normally requires
the best, most competent farmers are likely to try determinationofthemaximumtolerateddose(MTD)in
organic farming and probably only on a few of their rodents.Dosesslightlylowerthanthisfigureareusedto
fields. Therefore competent management will merely be extrapolate linearly to a concentration at which
transferredfromonekindoffarmingtoanotherwithno observed effects would be limited to one in a million
overall improvement. of the population and a ‘‘safe’’ exposure for the public
As stated earlier, the simplest comparisons between setatfigures100-foldlowerthanthis.Thusthesafelevel
organic and conventional agriculture is to use the same is frequently 10(cid:1)5–10(cid:1)6 the MTD and on theoretical
farm run by a farmer of excellent managerial quality. groundsitisveryunlikelythatthesamecellularreceptor
There are several established UK examples in the 10 (binding) sites could be occupied and the same effect
year experiment at Boarded Barns, Ongar, Essex induced, varying only in degree. Most cellular binding
(Boarded Barns, 2000; Higginbotham et al., 2000) and sitesgofromnullsaturationtofullsaturationovera30–
the7-yearexperimentatCooperativeWholesaleSociety 50-fold change in dose, not one million. The effects at
(CWS) farms at Stoughton, (Leake, 1997, 1999a,b, high dose are therefore a priori expected to be
2000a,b). Long-term experiments at Broadbalk, qualitatively different from low dose and the effects of
Woburn and Saxmundham may also be informative toxicity or cancer of little consequence to public
(Johnston, 1991; Rasmussen et al., 1998; Russell and exposure (Ames and Gold, 2000). Ames and Gold
Voelcke, 1936). There have been comparisons in other (1999) indicate that the carcinogenic effects of many
countries (Rasmussen et al., 1998) but climate and soil chemicals at MTD are really the result of induction of
differences make these less useful in an article primarily cell division which normally occurs only at high dose.
directed to UK farming. The public attitude towards synthetic pesticides
It takes decades to assess the effects of changes in derives from the views of Rachel Carson (1962).
agricultural practice and disadvantages of organic Unfortunately anecdotal evidence forms much of the
farming could take this length of time to appear. Many basis of Carson’s book and a number of simple errors
countriesintheworldpracticeorganicfarmingnow;but have been identified (Van Embden and Peakall, 1996).
not by choice, but from poverty. When the UK was While Carson’s book helped alert to the impact of
recognisably organic in the past (1900 for example), life agricultural techniques at the time on the environment,
expectancy was much lower, yields were lower, a her primary misunderstanding resulted from the claim
substantial segment of the UK population were mal- that ‘‘for the first time’’ the human population was
nourishedand/orateapoordiet.Foodinrealtermswas exposed to chemicals (pesticides) from birth to death.
much more expensive. In 1900, for example, 60% of Plants synthesise an estimated 10,000 chemicals whose
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function is to kill or deter insect pests and occasionally the introduction of pesticides and use through 50 years
larger herbivores. These natural pesticides are found in on life expectancy or on general public health (Coggon
allfruitandvegetables;whentestedatMTDtheyprove and Inskip, 1994).
to be equally as damaging as synthetic pesticides (Ames
andGold,1999,2000).Furthermorethedailyconsump- 2.2. Agricultural exposure to pesticides and cancer
tion of natural pesticides or carcinogens outweighs the
tracesof synthetic pesticides consumed by thepublic by Specific synthetic compounds have been linked to
many thousands to one. Mankind has always been cancer as a result of occasional high level of occupa-
exposed to ‘‘dangerous’’ chemicals and since many tional exposure (such as benzene on Turkish shoe
current crops have only recently been used as food and makers) or accidents such as Bhopal. In order to link
arealso theresult ofextensiveplantbreeding, thekinds together public exposure and cancer there must be
of natural chemicalto which we are now exposed istoo correlations between the level of exposure and the
recent to allow for biological evolution to have ensured magnitude of the response, consistent results from a
safe consumption (Ames and Gold, 1999). Solanine, number of different studies, and biological plausibility
chaconine, cucurbitacin, psoralen and genestein in basedonstudiesinlaboratoryanimals.Ifthereissucha
potato, cucurbits, celery and soy have all been shown relationship, it can be hypothesised that it should be
to have physiological effects if slightly elevated in food most readily apparent between cancer rates and those
(Trewavas and Stewart, 2003). most exposed to pesticides.
Carson (1962) alerted in her book to the potential Since farmers, foresters, pesticide users and manufac-
effects of DDT accumulation through food chains, to turers are by occupation more likely to be exposed to
observed eggshell thinning and thus brood failure of higher pesticide hazards than the general public, many
predatory birds. Attempts to repeat these observations published studieshave investigated cancer rates in these
in the laboratory failed (Wildavsky, 1995). However groups usually through cohort investigations using
because organochlorines like DDT are environmentally matched controls from the public particularly in age
stable,bansonitsusewereinstitutedintheearly70’s.In and social status (Blair and Zahm, 1991; Blair et al.,
westerncountriesDDTwasreplacedbyeffectivebutfar 1993;Dichetal.,1997;Faustinietal.,1993;Maroniand
less stable pesticides. But pressure on developing Fait, 1993; Wiklund and Dich, 1995. Of 12 separate
countries to do the same led to enormous increases in investigations on farmers involving in total about
malaria, a disease that particularly kills young children 300,000 people, 11 found that farmers had overall
(Attaran and Maharaj, 2000; Simon, 1996). In develop- cancer rates very substantially lower than the general
ing countries, cheap DDT also killed many crop and public. Slightly smaller numbers of investigations on
other human disease insect vectors and lowered food pesticide users and foresters revealed a similar (8 out of
prices that benefited the poorest most. Recent evidence 11) trend whilst only with manufacturers were cancer
has revealed that organochlorines are formed in rates similar to those of the members of the public. The
substantialamounts(mg/kg)indecayingplantmaterials reasons why farming is so healthy are not known but
such as crop roots in soil (Myeni, 2002). Because these data indicate not only a null result for the
organochlorines are fat soluble, they will be found in hypothesis relating pesticide exposure to cancer but a
allplantfoodmaterialsandmankindhasthereforebeen consistent result for the alternative, that pesticide
exposed to these stable chemicals probably throughout exposure may protect against cancer. These results are
evolutionary history and so far as is known without also consistent with a hormetic effect of low pesticide
effect. In fact any natural pesticide can bio-concentrate doses(seelater).Farmersdohavehigherratesoftheless
like DDT if it is fat soluble. Potato contains the fat common lymphoma but evidence indicates that lym-
soluble neurotoxins, solanine and chaconine, and high phoma is unrelated to pesticide exposure (Cantor et al.,
doses of these have been shown to cause birth defects 2003). Higher exposure to animal disease viruses or
(Ames and Gold, 1999). fungal disease may be a more plausible hazard.
However chemophobia is the commonest reason for Cancer death rates in the UK are in decline
the public to buy organic food on the assumption that particularly when lung cancer induced by smoking is
such food is free of synthetic pesticides. Organic food removed from the 50 years of detailed age-related
containssyntheticpesticidetracesalthoughunderstand- statistics published by the epidemiologists Coggon and
ably the amounts are lower than in conventional Inskip (1994). They conclude ‘‘there is no evidence that
produce (Baker et al., 2002). pesticides have had a major impact on overall rates of
Life expectancy continues to increase unabated cancer’’.Cancerratesincreaseover100-foldbetweenthe
(Oeppen and Vaupel, 2002) and figures specific for the ages of 20–70. Thus increased numbers of cancer cases
UK are to be found in Lomborg (2001). Centenarians accompany an increasingly healthy population domi-
are now ten times more common in the UK than they nated by elderly people. Only when cancer rates (cases/
were 50 years ago. There has been no obvious effect of numbers of people) are expressed for each defined age
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762 A.Trewavas/CropProtection23(2004)757–781
group as shown in Coggon and Inskip (1994) for every neo natal rat) about 3% normal circulating level of
5 years of age are genuine trends detectable. oestrogen in the non-menopausal female. The current
Although cancer death or cancer incidence, could be dietaryexposureofdibutylphthalatefromplasticwould
examined, it was common 50 years ago for pathologists increase circulating oestrogen-mimic content by
to report that coronary fatalities also had advanced 0.0006% and from dioxin and organochlorines by
cancer.Asfatalitiesdiminishfromheartfailuremoredie 6(cid:2)10(cid:1)6%, (Nilsson, 2000; Safe, 1998). In contrast the
from cancer. The estimates of human recovery from levels of oestrogen mimics in certain alternative medi-
cancer do not seem to be above 5–10% of diagnosed cines is sufficient to cause physiological changes in
cancers, so although incidence might be considered a treated men (Nilsson, 2000).
more useful criterion of environmentally damaging Concern over the consumption of soy genestein
materials, death rates may be considered a more valid, particularly in vegetarian diets using soy milk for pre-
easily diagnosed measurement (Coggon and Inskip, puberty children has been raised. Genestein is an
1994). It is among the young and middle aged that established genotoxin (Snyder and Gillies, 2003) and
anything untoward concerning illness first appears evidence from human studies suggests potential mod-
(Doll, 1992) and these two groups show the greatest ificationsofthyroidfunctionleadinginthelongtermto
declines in cancer rates over the last 50 years. Some goitre (Doerge and Sheehan, 2002).
cancers such as breast cancer are increasing but the
factorsthatconspiresuchaslifetimeoestrogenexposure
and most significantly obesity (Callee et al., 2002) are
the probable major risks (Safe, 1998, 2000). The
stomach is the most likely tissue substantially exposed 2.4. A diet high in fruits and vegetables cuts cancer rates
to ingested pesticides but stomach cancer rates have in half
declinedbyabout60%inthelast50years(Department
of Health, 1998). Blocketal.(1992)summarisesome200investigations
The Government’s Committee on Carcinogenicity on diet and cancer using cohort studies over the
(COC, 1999) after examining the evidence in detail previous 20–30 years. These authors indicate that for
concluded that breast cancer rates are completely virtually all the major cancers, a diet high in fruit and
unrelated to organochlorine exposure. Of the 43 vegetablescutscancerratesapproximatelyinhalf.These
separate investigations that I have found on this issue investigations involved very large numbers of people,
(lists are to be found in Gammon et al., 2002, Attaran onlyinwesterncountries,andthoseunderinvestigation
and Maharaj, 2000, and see Safe, 1995, 1998, 2000) at consumed conventional produce containing the inevi-
least 80% find no relationship at all and these include table pesticide traces. The fact that increased consump-
some very large surveys involving hundreds of thou- tion of these supposedly damaging substances in fruit
sands of women. Those that find some slight relation- andvegetablesactuallymakesyouhealthier,contradicts
ship are usually very limited in scope and fail on the any simple assumptions concerning pesticide traces and
grounds of consistency (Attaran and Maharaj, 2000), a cancer.
conclusion supported by Smith (2000) discussing in Furthermore we now know that fruits and vegetables
detailthetoxicityofDDT.Perhapsmoreintriguingwith contain an estimated 10,000 secondary products. When
the large investigations involving 50–150 thousand testedinexactlythesamewayassyntheticpesticides, at
women, cancerous tissue has slightly less DDT, DDE the MTD, 60% of each were carcinogenic (Ames and
the main metabolite and PCB’s although the difference Gold, 2000). But a number of these like limonene,
is within the standard error. The issue of DDT traces is perillyl alcohol, quercetin, allyl isothiocyanate, all
primarily concern about bio-accumulation rather than carcinogenic in high doses are now used to treat cancer
known toxicity. but at low doses. (The notorious poison, arsenic, has
also been used to treat leukaemia, (Trewavas and
2.3. Possible xeno-oestrogenic effects of pesticides Stewart, 2003). These natural pesticides (so-called
because they are synthesised by plants to poison insects
During the last decade there has been debate about a and herbivores) will also be consumed in greater
potential new threat to human health, exposure to amounts with diets high in fruit and vegetables. The
chemicals potentially with endocrinologic activity; the quantityonaverage consumed/dayofnaturalpesticides
so-called ‘‘endocrine disrupter’’ hypothesis. However outweighs synthetic pesticide residues by 20,000 to 1
measurements place this argument in perspective. The (Ames and Gold, 1999). These results indicate that the
major dietary source of oestrogen-mimicking molecules tests and assumptions, used to identify synthetic
are flavanoids and isoflavones in fruit and vegetables pesticidetracesasdamagingtohumans,lackmeaningful
(Nilsson, 2000). The daily consumption, about 1–2g/ interpretation since consumption of natural pesticides
day,representsoestrogenequivalents(determinedinthe does not induce cancer.
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2.5. Hormesis indicates the potential value of synthetic in turn destroying pre-neoplastic loci. Well-established
chemicals in the diet cases show that low doses of chemicals like cadmium
(Waalkesetal.,1988)ordioxins(Kocibaetal.,1978)or
Hormesis is the paradoxical effect of toxic chemicals anthracenes (O’Gara et al., 1965), for example, actually
at low concentration (Calabrese and Baldwin, 2001, lowercancerratesbelowcontrollevels.Inotherwordsif
2002, 2003a,b; Trewavas and Stewart, 2003). Many syntheticpesticidetracesareataleveltohaveanyeffect
toxins at high concentration are likely to have the at all (and they probably are not), the effect is as likely
opposite (and thus probably beneficial) effect at low beneficial as anything. The expected hormetic effect of
concentrations. There is an enormous toxicological natural pesticides in fruit and vegetables potentially
literature on this subject and Calabrese and Baldwin accounts for their beneficial action in reducing cancer.
(2003a,b)refertohormesisasarevolutionintoxicology.
The standard method of assessing toxicity was based 2.6. The price of fruit and vegetables determines health
on a model of cancer that is now outdated. This model
assumed that toxic at high concentration simply meant Organic food is more expensive because it uses land
less toxic at low and that there was no threshold below less efficiently, as will be seen later. However only 21%
whicheffectsofpesticideswereabsent.Consequentlyno ofthe UK and only20%ofUS citizens actually eatthe
concentration of any toxin could be considered abso- necessary two fruit and three vegetable portions/day
lutely safe. The theory became known as the linear no- recommended by respective governments to provide
threshold theory (LNT) and was formulated in the minimal protection against cancer (as indicated by
1970s. Developments in our understanding of cancer Blocketal.,1992).Thosenumberswillnotbeincreased
have shown the basic assumptions (all mechanisms of by raising the price of produce because it is known that
cancer the same; cancer as a monotonic disease) that price is a very strong determinant of consumption
under-pinned the model are incorrect. (Knutson, 1999; Lutz and Smallwood, 1995). Further-
Insteadmanychemicalsinthelowdoseregionhavea more raising the price will not encourage the cultural
dose response curve that is J-shaped, indicating, for change necessary to increase fruit and vegetable
example and where relevant, that low toxin consump- consumption. For those on low incomes, if organic
tion actually inverts the physiological effects of high food is purchased less will be consumed, with con-
dose(TrewavasandStewart,2003).Datacollectedfrom sequences in cancer rates decades later.
5000 dose response measurements (abstracted from
21,000 papers) indicate that low doses of many 2.7. Conclusion on pesticides and cancer
supposedly toxic chemicals, metals, pesticides, fungi-
cides, petroleum fractions, radiation and even diluted On current views low levels of synthetic pesticide
factory effluent either reduce cancer rates below traces could have beneficial effects on health but much
controls, increase longevity or growth in relevant moreanddifficultresearchisneededtoclarifythisissue.
organisms (Calabrese and Baldwin, 2003b). Becauseconventionalfoodisalsocheaperandincreased
There are many familiar examples of hormesis. consumption has improved the health of the UK
Aspirin, where one or two tablets/day improve the population, conventional food can be regarded as
circulation, but 30 will stop it altogether. Virtually all healthier than organic food. The fact that stomach
pharmaceuticals are similar. Fluoride to strengthen cancer rates have declined by 60% in western countries
bones and teeth but fatal in large doses. Antibiotics since 1950 is ascribed to the fact that conventional fruit
and vaccines where a 10-fold higher than recommended and vegetable consumption has doubled during that
dose can kill. Sunshine induces vitamin D formation in period. Furthermore the epidemic of allergy disorders
small doses, but melanoma in large doses. Radon, a including asthma in the UK is increasingly being
radioactive gas formed in higher amounts in granite suggested to result from environments which are too
houses but those who live in such houses have lower clean. Removing beneficial chemical traces from food
ratesoflungcancer(Pollycove andFeinendegen, 2001). that help potentiate and energise the immune system
Vitamin A is necessary for vision but teratogenic at might make matters worse for health. As hunter-
slightly higher than recommended doses (Kuiper et al., gatherers, mechanisms like hormesis would have been
2001). Insulin is the crime writer’s invisible murder essential to enable humans to eat a diversity of food in
weapon at high dose, but necessary to control human variable condition but without long-term health da-
blood glucose level at low dose. Drinking water mage. We have good defence mechanisms to deal with
suddenly in very large amounts has been known to kill low doses of chemicals in our diet. Pesticides keep fruit
by upsetting the ion balance. andvegetablescheaptherebyencouragingconsumption.
Hormesis is thought to result from the beneficial The primary problem with pesticides is that they do kill
effects of mild chemical stress at low concentration insects other than those which are pests and which can
potentiatingtheimmuneandoxidative defencesystems; be beneficial. The eventual evolution of pesticide
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resistance constrains their agricultural value. However Table1
careful use of pesticides as in IFM can greatly prolong Acomparisonofthehumanandecotoxicityofmancozebandcopper
their usability and transfer to these kinds of farming sulphate
systemshouldbeencouraged(VanEmbdenandPeakall, Mancozeb Copper
1996). A technology that improves natural crop
Humanhealth
resistance reducing pesticide use, such as GM insect-
LD >5000mg/kg 50mg/kg
50
resistant crops, should be beneficial. EPAclass Practicallynon-toxic Corrosiveandtoxic
Much of the antagonism against pesticides assumes Healtheffects Non-toxicbyoralroute Kidneyandliverdamage
that mankind is the only organism releasing chemicals
Ecotoxity
intotheenvironment.Howeverasorganismswepossess
Earthworms Lowtoxicity Verytoxic
a unique faculty, that of high intelligence; a natural
Birds Low Moderatelytoxic
property that can be used for benefit or damage as Smallmammals Non-toxic Harmful
anything else in nature. Every organism releases DT soil 6–15days Non-degradable
50
chemicals into the environment and the soil. The most
MancozebisasyntheticcopperfungicideusedfortreatingPhytophora
obviousareoxygen,methane,nitrousoxide,DNAupon
infestans (potato blight) in particular, and its organic equivalent is
death,urineandotherexcretedproductsamongstmany copper sulphate. The full table can be found in Leake (1999a).
thousands. Isoprene emitted in enormous amounts by Mancozebisclearlylessdamagingthancoppersulphate.
trees (about 400Tg/year) modifies local climates Anyorganicpesticidehasa1in2chanceofbeingcarcinogenicathigh
concentrations(AmesandGold,1999,2000).
(Fuentes et al., 2000). Many plants also release
numerous secondaryandpoisonousproducts,including
allelopathic compounds, into the soil environment, copper sulphate. The full table can be found in Leake
aimedatkillingotherorganisms.Thepublicsupposition (1999a). In environmental qualities, mancozeb is super-
that synthetic pesticides are dangerous because they kill ior in all categories compared to copper sulphate. In
insects fails to recognise that natural pesticides, that we termsofhumanhealth,coppersulphateiscorrosiveand
consume every day in abundance, do exactly the same toxic and has caused liver disease in European vineyard
thing. Fungal and blue green algal toxins are well workers. Although the EC theoretically banned copper
known. Few of these ‘‘natural’’ chemicals are ever sulphate in 2002, no alternative has been found for
looked for in human beings and it is perhaps time that organic farmers and thus it continues to be used. The
they were; the public perspective might then change. consequences of not using copper sulphate properly
have been reported as organic farms acting as reposi-
2.8. Where organic naturalism ideology leads tories of late blight, a serious disease of potato (Eltun,
1996; Zwankhuizein et al., 1998) or seriously damaged
Acommonclaimisthatintensiveagricultureseeksto orchards(VanEmbdenandPeakall,1996).Anysensible
dominatenaturewhereasorganicagricultureworkswith approach would determine use based on toxicity.
nature. It is not very clear what the statement means Otherorganicpesticidessuchassoap(producedfrom
sincenoformoffarmingisnaturalrelyingineverycase animal fat with alkali) hardly merits the term natural.
on clearing ground and destroying the natural environ- Rotenone, another organic pesticide, has been recently
ment (forest and the associated organisms) that was associated with Parkinsons disease, and another, Bt
there before. spores, used to kill insects has been associated with
Howeverthephraseusestheterm‘‘nature’’,appealing damaging respiratory effects (Trewavas, 2001). Syn-
toacommonphenomenondescribedbyE.O.Wilsonas thetic pyrethroids can be as unstable as the organic
Biophilia. Human beings recognise the natural world pesticide, pyrethrum, but work at much lower concen-
and often feel a strong kinship with it because we are trations.Hownaturalaretheorganicpesticidessulphur
living organisms too. Simplistically this turns into or oil when they have to be mined, chemically modified
‘‘natural’’ equated with ‘‘good’’ and human activity as or distilled before use?
‘‘synthetic’’ equated with ‘‘bad’’. This view is self Agriculture tends in one sense to mimic the effects of
evidently, a version of original sin. However child individual tree loss in forests. When a mature tree falls
death, starvation, plague, cholera or even SARS are all over, light penetrates the forest floor, there is flush of
theresultsofnaturalactivities;andincontrast,synthetic nitrate and water in the soil. Weed seeds, which are
activities, such as architecture, painting, music and sensitive to light and/or nitrate, germinate. Most crops
literature are all man-made. are derived from weeds although their germination
The limitations of this view can be exposed by requirements for nitrate and light have been bred out.
comparing a natural pesticide with its synthetic equiva- Farmers mimic tree loss by clearing ground. The
lent. Table 1 makes some limited comparisons between assumption that nitrate is somehow an un-natural
mancozeb, a synthetic copper fungicide usually used to fertiliseriscontradictedbythisperfectlynaturalprocess.
treat late blight, and the organic pesticide equivalent, Butthefarmingactivitymostdeservingthetermnatural
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A.Trewavas/CropProtection23(2004)757–781 765
is no-till agriculture which mimics in part the annual ing the necessity for twice as much land to achieve that
cycle of the meadow or prairie. yield (Sinclair and Cassman, 1999). The Boarded Barns
(2000) study routinely reported organic wheat yields
using animal manure of about 50% conventional
3. Comparisons of organic and conventional soil production. Winter wheat is still the staple of most
properties UK arable farming.
Such yield differences indicate that organic farming
usesgoodfarmlandlessefficiently.Insteadanequivalent
The development of thin film technology several
yield to organic farming could be achieved on less
decadesagoforgrowinggreenhousecropsdemonstrated
conventional farm land and the remainder (20–50% of
that soil is not actually essential for good crop growth
the farm) more profitably employed as woodland, or in
and that only minerals are actually required for active
willow plantations for bio-fuel (Bertillson, 1992; Tre-
and healthy plant growth (Jones, 1982). Aeroponics
using misted mineral solutions generates the most wavas, 2001), (thus recycling carbon) or returning it to
abundant and healthy root systems (Soffer and Burger, other natural conditions such as fenland. These con-
siderations of efficiency are much more important
1988). Nevertheless most crops will continue to be
overseas where growing populations using inefficient
grown in soil.
organic agriculture, will simply cut down more tropical
forest than they need to feed the growing population.
3.1. Is a low organic yield more natural?
Currently, for example, Mexican peasants destroy 3
million acres of virgin tropic forest/year to slash-and-
From many reports it is clear that organic yields are
burn agriculture (Gregory et al., 2002).
usually lower, the extent depending on the crop. Leake
However the UK government has signed up to a
(1999a,b, 2000,a,b) at CWS agriculture using fields at
protocol to ensure that 10% of all fuels used in the UK
the same farm reported that organic wheat, beans and
by2010comefromnaturalsourcessuchasethanol,thus
peas yields were 60–70% whereas oats were 85%
ensuring that carbon is recycled. On this basis wheat is
conventional yields (Table 2). Such measurements have
likely the source for fermentative ethanol production
been repeated on numerous occasions with variable
and increasingly, intensive agriculture the likely means
results. Usually organic yields are much lower but
for its production.
occasionally they can match conventional productivity
inasingleyear.Butmostorganicfarminginvolvesaley
3.2. Why are organic yields lower?
period in which clover or alfafa and grass is grown to
allow nitrogen fixation and provide the soil with
One reason has to do with the prohibition on the use
nitrogenonceploughedin.Noorganicyieldisobtained
of very soluble fertiliser. There is a major surge in crop
throughout the ley period unless it is grassed and used
growth suddenly in late spring and mainly in leaf
forcattle,whereasinaconventionalfarmthesamefield
production.Leavesarethemostnitrogen-richtissueina
can be in use continuously for arable crops. Many
higher plant and consequently there is a relatively
organic farmers use a field twice for arable crops after
sudden heavy requirement for nitrate to produce leaf
the ley period and since in the second year less nitrogen
protein for chloroplasts and photosynthesis. The vege-
is available, the yield further diminishes. Thus occa-
tative reserves laid down during canopy expansion help
sional claims that yields can be the same as a
provision theseeds when they form. Therefore maximal
conventional farm may only be true one year out of
seed yields are likely to be obtained only when the
three. It is important to compare total yields over a
provision of soil nitrate and the associated crop
number of continuous years, not on a single year. Thus
requirements for leaf production are synchronised. This
Drinkwater et al. (1998) claimed that organic and
temporallyunevenrequirementforNinspringtimeonly
conventional corn yields were identical without clarify-
can be matched by careful application of very soluble
fertiliser.
Table2 However a process that ploughs in material which is
Typical yields of the major crops grown conventionally and on Soil only slowly degraded over many months or even years
Association licensed organic fields on the same farm and using the
cannot release minerals in the short intense burst as
samefarmer
required for plant growth. Provision of nitrogen by
Winter Winter Winter Dried decay of organic material (mineralization) throughout
wheat oats beans peas
the season produces nitrate when it is little needed and
Organic 4.82 4.87 2.60 2.13 does not provide sufficient when it is. Furthermore
Conv. 7.12 5.75 3.60 3.47 mineralization is greatly speeded up when the field is
ploughed, months ahead of the time required by the
Leake(1997,1999b).CWSexperiments,1989–1996.
DatacompiledfromLeake(1997,1999b). crop.
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766 A.Trewavas/CropProtection23(2004)757–781
10 to provide the conditions required for plant growth’’, a
%) 2.5 -1ha view echoed by Russell and Voelcker (1936) much
Gria nN ( 2.0 ain yield t. Oavregraangice emhaaorvldiineifrgy.dGpiflifavenerentngtthrooepwtcitmohmaalpnsleodxilityryieeqlodufiraseonmidlenawttsti,rthiibtuiestaedcsohuwbchtrifocuhpl
1.5 5 Gr if a more precise definition can be constructed.
Critically, crop plants interrogate the soil in which they
0 100 200 300
kgNha-1applied live and then respond accordingly. In the wild, many
types of soil are occupied by individual species, and
Fig. 2. Does the supply of available nitrogen restrict organic
plants have developed necessary control systems to
productivity? The graph shows estimates of wheat grain N (%) and
grain yield against N applied to the soil. The organic average yield mitigate some of the variations they come across. If
obtained when the organic soil measurably contains 300kgN/ha is conventionalsoilswerepoorfromaplantpointofview,
indicatedbyanarrowandsuggeststhatmostNinorganicfieldsisnot thiswouldresultinpooryieldsandclearlytheyarenot.
availablewhenthecropmostneedsitinspring.Thefigureisadapted
After a detailed consideration of soil organic matter,
fromBerryetal.(2002).
minerals and nutrients in labile mineral pools in soils,
Stockdale et al. (2002) also conclude that ‘‘Although
nutrient management in organically managed soils is
In a detailed examination of mineral availability, fundamentally different to soils managed convention-
Berry et al. (2002) determined the grain N as a % in ally,theunderlyingprocessessupportingsoilfertilityare
wheat, the grain yield and inorganic fertiliser applied not’’. But ploughing in of legume rotations in organic
(Fig. 2). Their comment is that although the amount of farming provides substantial amounts of soluble miner-
N in organic soils should be equivalent to 300kgN/ha als to the soil since the vacuole of each cell of a mature
based on soil analysis, organic wheat plants act as plant contains mM concentrations of soluble calcium,
though there is only about 50kgN/ha available for magnesium,phosphateand2–300mMpotassiumchlor-
growth and seed formation. Berry et al. (2002) also ide. Therefore the nutrient management processes are
indicate that the common practice of applying manure not completely different.
or slurries to ley legumes simply diminishes the amount
ofNfixedbythelegumesresultinginawasteofmanure. 3.4. Is organic soil structure better?
Morecrucially these measurementsindicatethat overall
analysisofNonorganicsoilsismisleadingwhensucha The assumption is that organic farms using organic
mismatch between unavailable and available N is so material added back to the soil must produce a better
clear. It also suggests that excess N in organic soils, as soil.Itshouldbeaddedthatthecriteriausedtodefinea
reported by Watson et al. (2002), appears at the wrong good soil are those of the soil scientist, not that of the
time of year and is likely to disappear into waterways individual crop plant which may have a very different
and courses since it remains unused by the crop. Since perspective.
organic regulations stipulate the use only of supposed However a review of the literature and an examina-
natural minerals that decay slowly and are therefore tion of some 30 soils in the UK in organic and
weakly soluble, general mineral analysis might well conventional farms by Shepherd et al. (2002) led to the
prove entirely misleading as to how much mineral such conclusion ‘‘it is not the farming system per se that is
as phosphate is actually available to crop plants during important in promoting better physical conditions but
the current season. the amount and quality of organic matter returned to
Ecologists regard fitness as usually measurable in the soil’’ Surprisingly few differences in organic matter
terms of seed yield (Bazzaz, 1996). On this ecological contentwerefoundbetweenorganicandconventionally
basis, conventional farming produces fitter plants than managed pasture soil, and only trivial differences in
organic agriculture. 20% of the soils between conventionally managed and
organically managed arable soils were detected, usually
3.3. Is soil fertility better on organic farms? it seems on stockless conventional farms where differ-
encesmightbemorelikely.Thereisalargebackground
One of the claims of organic agriculture has been the of soil organic matter regardless of farming system
supposed benefits of organic regulations to soil fertility deriving from crop roots and root exudates.
and soil structure. A series of reviews on organic soils No consideration seems to have been given in the
constructed by organic and conventional researchers reviewed literature to the need for careful matching of
and published in Soil Use and Management 2002 managerial standard in the comparisons made by
(Vol. 18 supplement) clarifies the situation. The con- Shepherd et al. (2002). But best-practice, mixed IFM
cludingandsummarisingchapter(Stockdaleetal.,2002) farms will equally apply manure to the soil when they
states that ‘‘Soilfertility isdefined as an ability of a soil have it and in this case no meaningful difference
Description:Aeroponics using misted mineral solutions generates the most abundant and healthy root systems (Soffer and Burger,. 1988). Nevertheless most crops will continue to be grown in soil. 3.1. Is a low organic yield more Atrazine and simazine in runoff from conventional and no-till corn watersheds. Agri