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Animal(2013),7:6,pp1028–1043 &TheAuthors2012.TheonlineversionofthisarticleispublishedwithinanOpenAccessenvironmentsubject totheconditionsoftheCreativeCommonsAttribution-NonCommercial-ShareAlikelicence,http://creativecommons.org/licenses/by-nc-sa/2.5/.. animal ThewrittenpermissionofCambridgeUniversityPressmustbeobtainedforcommercialre-use doi:10.1017/S1751731112002418 Prospects from agroecology and industrial ecology for animal production in the 21st century B. Dumont1-, L. Fortun-Lamothe2, M. Jouven3, M. Thomas4 and M. Tichit5 1INRA,UMR1213Herbivores,Theix,63122Saint-Gene`s-Champanelle,France;2INRA,UMR1289TissusAnimauxNutritionDigestionEcosyste`meetMe´tabolisme, 31326Castanet-Tolosan,France;3SupAgro,UMR868Syste`mesd’ElevageMe´diterrane´ensetTropicaux,34060Montpellier,France;4Universite´deLorraine-INRA, USC0340AnimaletFonctionnalite´sdesProduitsAnimaux,54505Vandoeuvre-les-Nancy,France;5INRA,UMR1048Sciencespourl’ActionetleDe´veloppement: Activite´s,Produits,Territoires,75231Paris,France (Received4April2012;Accepted12November2012;Firstpublishedonline21December2012) Agroecologyandindustrialecologycanbeviewedascomplementarymeansforreducingtheenvironmentalfootprintofanimal farmingsystems:agroecologymainlybystimulatingnaturalprocessestoreduceinputs,andindustrialecologybyclosingsystem loops,therebyreducingdemandforrawmaterials,loweringpollutionandsavingonwastetreatment.Surprisingly,animalfarming systemshavesofarbeenignoredinmostagroecologicalthinking.OnthebasisofastudybyAltieri,whoidentifiedthekey ecologicalprocessestobeoptimized,weproposefiveprinciplesforthedesignofsustainableanimalproductionsystems: (i)adoptingmanagementpracticesaimingtoimproveanimalhealth,(ii)decreasingtheinputsneededforproduction, (iii)decreasingpollutionbyoptimizingthemetabolicfunctioningoffarmingsystems,(iv)enhancingdiversitywithinanimal productionsystemstostrengthentheirresilienceand(v)preservingbiologicaldiversityinagroecosystemsbyadapting managementpractices.Wethendiscusshowthesedifferentprinciplescombinetogenerateenvironmental,socialand economicperformanceinsixanimalproductionsystems(ruminants,pigs,rabbitsandaquaculture)coveringalonggradientof intensification.Thetwoprinciplesconcerningeconomyofinputsandreductionofpollutionemergedinnearlyallthecasestudies, afindingthatcanbeexplainedbytheeconomicandregulatoryconstraintsaffectinganimalproduction.Integratedmanagement ofanimalhealthwasseldommobilized,asalternativestochemicaldrugshaveonlyrecentlybeeninvestigated,andtheresults arenotyettransferabletofarmingpractices.Anumberofecologicalfunctionsandecosystemservices(recyclingofnutrients, forageyield,pollination,resistancetoweedinvasion,etc.)arecloselylinkedtobiodiversity,andtheirpersistencedependslargely onmaintainingbiologicaldiversityinagroecosystems.Weconcludethatthedevelopmentofsuchecology-basedalternatives foranimalproductionimplieschangesinthepositionsadoptedbytechniciansandextensionservices,researchersand policymakers.Animalproductionsystemsshouldnotonlybeconsideredholistically,butalsointhediversityoftheirlocal andregionalconditions.Theabilityoffarmerstomaketheirowndecisionsonthebasisoftheclosemonitoringofsystem performanceismostimportanttoensuresystemsustainability. Keywords: aquaculture,environmentalfootprint,farmingsystems,inputs,livestock Implications design sustainable faming systems adapted to this context. Promoting systemic analyses and elaborating on the diver- Although animal farming systems undeniably contribute to sity of local and regional conditions are key elements of improvinghumanconditionbyprovidingproteinsfornutrition these promising approaches, the implementation of which andincomeforruralpopulation,theycanalsoberegardedasa willrequire changing theposition and methods adoptedby majorcauseofworld’smostpressingenvironmentalproblems. farmers,extensionservices,researchersandpolicymakers. Animalproductionisandwillincreasinglybeconstrainedby competition for natural resources, changing sociocultural Introduction values and by the need to operate in a carbon-constrained economy. Agroecology and industrial ecology can help to Recent decades have seen interesting turns to alternative farming systems in response to growing ecological concern -E-mail:[email protected] over industrial agriculture. These numerous alternatives for 1028 Ecology-basedalternativesforanimalproduction re-greening agriculture (Rockstro¨m and Karlberg, 2010; demandsonwater,pollutionandbiodiversitylosseshaveall Koohafkan etal., 2012) span notions or concepts such as putlivestockfarminginabadlight(FAO,2006).However,as ecological or sustainable intensification of agriculture, high underlined by Gliessman (2006), the problem lies not so nature value farming, eco-agriculture, biological farming, muchwiththeanimalsthemselvesbutratherwithhowthey green agriculture, organic farming and more. They promote are incorporated into agroecosystems and food systems. ways to reconcile natural resource management, food pro- Their disconnectedness from the land is probably the main duction and ecosystem services in the long term and under problem threatening the sustainability of animal farming climate uncertainty. They can also be seen as responses to systems. In the second edition of his book on agroecology, bothfarmerandconsumerdissatisfactionwiththenegative Gliessman (2006) devoted a chapter to the beneficial roles impactsofindustrialfarming.Inthis‘re-greeninglandscape’, animalsplayinagroecosystems:producingprotein-richfood the future for sustainable animal production is a subject for humans from inedible resources (e.g. crop residues, by- of debate. Steinfeld and Wassenaar (2007) argued that products, grasslands), providing ecosystem services (e.g. futureexpansionofthelivestocksectorwillrelyonintensive carbonsequestration,biodiversity),recyclingplantnutrients livestock systems, whereas Herreroetal.(2010) concluded andprovidingsocialbenefits. that more extensive integrated crop–livestock systems IndustrialecologyalsoemergedintheUnitedStatesdur- couldmakeamoresignificantcontributiontofoodsecurity. ingthe1980s(FroschandGallopoulos,1989;Frosch,1992). Godfrayetal.(2010)contendedthatitwouldbepossibleto As a scientific discipline, industrial ecology was defined as design livestock farming systems to reduce net greenhouse the study of material and energy flows through industrial gasemissions,whereasGilletal.(2010)pointedoutthatthe systems.It canalsobeseen asanewapproachtoenviron- evidence base connecting policy interventions and their mental management where technology is used to mitigate consequencesonlivestockemissionsstillremainsweak. the effect of these flows on the environment (Diemer and Despitethislimitedscientificconsensus,itisclearthatthe Labrune,2007).Inthisframework,rawmaterialandenergy overallfunctioningofecosystemsiscloselyintertwinedwith consumption is optimized and wastes are reused as inputs animalproductionfortwomainreasons.First,thelivestock for another production process. Industrial ecology is being sector is currently a major driver of land use. From 1961 to increasingly applied to livestock farming, in particular for 2001,morethan60%oftheworldmaizeandbarleyharvest manure management in large-scale intensive systems (Holm went to livestock feed (Food and Agriculture Organization Nielsen, 2010). Industrial ecology and agroecology can thus (FAO), 2006). Second, the type and amount of animal pro- offerabroadrangeofoptionsthatneedtobepursuedsimul- teins in human dietary patterns are important drivers of taneously.Ontheonehand,theapplicationofindustrialecol- agriculturalexpansion(Wirseniusetal.,2010).Theplaceof ogy to animal production can provide solutions to curb the animalfarmingsystemsinthere-greeningprocessdemands growingcompetitionforland,waterandenergy,whileadding recognition of their positive and negative contributions to quantitatively to food production. It will also offer solutions agroecosystem processes. It is also important to take into for the reduction of waste and its negative impacts on the account their diversity, as they cover long gradients of environment. On the other hand, agroecology targets a very intensification (ranging from grassland-basedto large-scale substantial proportion of grassland-based livestock systems intensive systems) and biogeographical conditions. Given andplaysanimportantroleinbiodiversityconservation(Veen this diversity, we believe that there is no single avenue for etal.,2009).Byconsideringbiodiversityasbotharesourceand reintegrating animal production into ecological thinking. an output in livestock systems, agroecology puts food and A dual perspective is needed, grounded in the principles ecosystem integrity at the same level of priority; it can thus of industrial ecology and agroecology as complementary provide alternative dual-benefit solutions through stimulating frameworks for exploring how to switch the net effects of naturalprocessesforinputcostreductionandincomegain. animalproductionfromstresstobenefits(Janzen,2011). Theaimofthisworkistoexplorepotentialroutesforthe Agroecology emerged in the United States during the development of ecology-based alternatives for animal pro- 1980sasascientificdisciplinethatappliesecologicaltheory duction. The first section proposes five principles for the to the design and management of sustainable agroecosys- design of sustainable animal production systems. These tems (Altieri, 1987; Gliessman, 1997; Wezel and Soldat, principlesarebasedonkeyecologicalprocessesproposedby 2009). Agroecological systems are expected to be produc- Altieri (2002) to be optimized for sustaining yields, while tive, to need few chemical inputs and to be resource con- minimizing the negative environmental impact of animal serving. In the early 2000s, Francis etal.(2003) redefined productionsystems.Theyareillustratedwithexamplestaken agroecology away from this rather narrow field scale and fromawiderangeofsystems.Thesecondsectionexamines toward a wider food system scale, as ‘the integrative study six case studies covering a long gradient of intensification, of the ecology of the entire food system, encompassing wherewehighlighthowthedifferentprinciplescancombine ecological, economic and social dimensions’. Despite the to generate environmental, social and economic benefits. recent surge in academic literature on agroecology, animal In the last section, we discuss how the founding principles production systems have been so far ignored in most of agroecology and industrial ecology can be mobilized in agroecological thinking (Gliessman, 2006). Processes such animalproductionsystems,andconcludeonperspectivesfor as land-use change, greenhouse gas emissions, increased promotingsuchecology-basedsystems. 1029 Dumont,Fortun-Lamothe,Jouven,ThomasandTichit Fiveprinciplesforthedevelopmentofecology-based relationtoperiodandintensityofnutritionalstress(Mandonnet alternativesforanimalproduction etal., 2011). Management of flock health in organic sheep farming systems benefits from rotational grazing, as nema- Ecology-based management of animal production systems todelarvaedeclineintemporarilyungrazedplots.Rotation- requires a deep understanding of the processes by which allygrazedornewlysownpasturesshouldthusbededicated agroecosystemscanproducefood,fiber,etc.moresustainably, tolambs,whicharemorevulnerablethandryewes(Cabaret, using fewer external inputs (Altieri, 2002). Altieri (2002) 2007).Asparasitesusuallydifferbetweenlivestockspecies, proposedasetoffiveecologicalprocessestobeoptimized: alternate grazing with cattle reduces parasite burden in (i) strengthening of the ‘immune system’ of agricultural sheep(MahieuandAumont,2009).Consumptionoftannin- operations (nurturing proper functioning of natural pest richplantsincludingsulla(Hedysarumcoronarium),sainfoin control), (ii) decreasing toxicity in the environment through and trefoil also reduces infestation by parasitic nematodes reduction or elimination of agrochemicals, (iii) optimizing (Hosteetal.,2006).Inthetropics,feedinglambswithwilted metabolicfunctioningofsoils(organicmatterdecomposition cassava foliage or banana foliage decreased nematode and nutrient cycling), (iv) balancing regulatory systems fecundity while providing suitable energy intake (Marie- (nutrient cycles, water balance, energy flows, population Magdeleineetal.,2010).Theseplantshavebeenshownto regulation,etc.)and(v)enhancingconservationandregenera- improve clinical status (diarrhea indices, etc.) and reduce tion of soil and water resources and biodiversity. To extend mortality under parasitic challenge, while limiting the need ecological thinking to animal production systems, we propose forchemicaldrugs(Paolinietal.,2005;Kidaneetal.,2010). five principles that are based on the application of these eco- In addition to a direct antiparasitic activity, they might also logicalprocesses,andillustratetheminawiderangeofsystems. have some indirect effects by increasing host resistance. Observations that sick ruminants were able to consume Adoptingmanagementpracticesaimingtoimprove substancesthatwerenotpartoftheirnormaldietandcon- animalhealth tained active ingredients capable of improving their health Applying agroecology to the question of animal health support the hypothesis that animals can self-medicate impliestofocusonthecausesofanimaldiseasesinorderto (Grade´ etal.,2009).Inpenstudies,lambsexperiencingnega- reducetheiroccurrence.Theuseofchemicaldrugsneedsto tiveinternalstatespreferentiallyconsumedfoodscontaininga be minimized as the dumping of medicine residues in the specific compound known to rectify their state of discomfort environment and the spread of resistance to antibiotics (Villalbaetal.,2006).Parasitizedlambsalsoslightlyincreased represent public health and environment issues. Major intakeof atannin-containingfoodwhenexperiencinga para- attentionwillthereforebegiventochoosinganimalsadap- site burden (Villalba etal., 2010). Self-selection of plant sec- ted to harsh environments and using a set of breeding ondary metabolites could thus hold a place in the quest for practicesthatfavoranimaladaptationsandstrengthentheir alternativestochemicaldrugsinpastoralsystems. immune systems. Adaptation of animals to hot climates Farming practices combining diet, housing and strain includesmallbodysize(andthusahighsurface/volumeratio choicetosimulatehostdefensesarecrucialforpigs,poultry to evacuate body heat), thin skin with little subcutaneous and rabbits, which are usually housed at high densities fat, little or no hair or feathers and behavioral adaptations, in intensive systems. Although maintaining animals in a such as night feeding (Mandonnetetal., 2011). Goats are clean,dryenvironmentisessentialtopreventthespreadof welladaptedtoharshenvironments,astheyexploitawide microbes,closetosterileconditionsmayalsoholdbackthe range of plant species, decrease their metabolic require- developmentoftheirimmunesystem.Atbirth,thedigestive mentsandrecycleureainresponsetosevereundernutrition tract is sterile and progressively colonized by flora of the andare ableto concentrate urineunderdrought conditions motherandoftheenvironment,whichexertsabarriereffect (Silakinove, 2000). In cattle, Bosindicusgenotypes faced against exogenous pathogenic bacteria, and stimulates the withfoodscarcityreactedtolong-termfoodfluctuationsby immune system (Rheeetal., 2004). Stringent hygienic con- mobilizingandrestoringbodyfatreserves,andwerelesssen- ditionsalteredthedevelopmentofdigestive microfloraand sitive thanB.indicus3Holstein cross-breds to metabolic dis- stimulated inflammatory response genes in pigs (Mulder ordersanddiseasesinthecommonfoodscarcityconditionsof etal., 2009). Conversely, the adoption at 1 day of age of thetropics(Jenetetal.,2006).Localspeciesorbreedsthathave renewal rabbit females by reproductive females permitted been selected in tropical environments are more resistant to the early implantation of a functional, diverse symbiote, trypanosomes,gastrointestinalparasitesandticks(Mandonnet whichincreasedrabbitresistancetopathogens.Dietaryfiber etal., 2011). Nematode resistance in sheep can be selected stimulated the activity of cecal microflora and provided an byaclassicalquantitativeapproach(Sechietal.,2009),which appropriate supplementation to ensure digestive comfort suggeststhatselectionprogramscouldextendthebenefitsof (Gidenne etal., 2010). In poultry, susceptibility to dietary usingadaptedgeneticresources. stresswasgeneticstraindependent(Hangalapuraetal.,2005), Adaptationtoharshenvironmentsalsorequiresfarmersto further emphasizing the importance of choosing genotypes adopt management practices that make the best possible adaptedtoparticularproductionobjectives.Breedingpractices use of livestock adaptations. For example, it is possible to shouldalsolimitsocialstress.Mixinganimalshasbeenshown choose the frequency and seasonality of reproduction in to suppress the immune response to a viral vaccine in pigs 1030 Ecology-basedalternativesforanimalproduction (DeGrootetal.,2001)andtoimpairgrowthinfinishingbulls andnaturalresources.Majorlimitationsofrangeland-based (Mounieretal., 2006). Appropriate breeding practices that feedingsystemsarethelargeareasrequiredtocompensate maintainstabledominantrelationshipsarelikelytoincrease for low forage productivity, which increases farm work socialtolerance,andtherebylimit both feedinputsandthe (fences or shepherding), and the seasonal and year-to-year useofchemicaldrugsinintensivesystems. variability in the amount and quality of forages (Jouven In aquaculture, controlling water quality is pivotal for et al., 2010). Alternative feed resources such as millet, health management. In intensive systems, an alternative to wheat, oat and barley straws are other cheap resources antibiotics is the use of probiotics and prebiotics adminis- that serve as supplemental feed for ruminants, horses and teredviathefeedordirectlyinwatertobenefitfishthrough donkeys in many agroecosystems around the world. In direct or indirect modulation of gut microbial balance, California, crops leave residues such as culled Brussels additional sources of nutrients and direct effects on water sprouts, waste tomatoes and carrot pulp after juice extrac- quality (Balca´zar etal., 2006). It can improve fish health tion,whichareusedtosupplementgrazinganimalsorforages status,resistancetodiseases,growthperformanceandbody (Gliessman, 2006). Various tropical forages make a viable composition (Merrifield etal., 2010): feeding turbot larvae alternativetosoybeanmealindietsforlambs(Archime`deetal., (Scophthalmusmaximus)withrotifersenrichedinlacticacid 2010)orgrowingpigs(Rodrı´guezetal.,2006).Draughtanimal bacteria (Lactobacillus and Carnobacterium sp.) provided powerforlandpreparationandtransportreducesenergyusein protection against a pathogenicVibrio, and increased their tropical farming systems. Because of competing demands on meanweightandsurvivalratecomparedwithcontrollarvae water for drinking, hygiene and energy, it is also urgent to (Gatesoupe,1994). improvewatermanagementinaquacultureandforcropforage irrigation. In aquaculture, a variety of technologies have been Decreasingtheinputsneededforproduction developed to offer solutions to limited water resources and Ahighproportionofarablelandisdevotedtosoybeansand degradation of water quality: these are recirculating aqua- cornforanimalfeeds,whichrequirechemicalfertilizersand culture systems (RAS; Martins etal., 2010), and integrated large quantities of water for irrigation. Thus, a major chal- intensiveaquacultureinstallationsthatcantakeplaceincoastal lengeisreducingtheinputsrequiredforproduction.Thiscan waters,offshoreenvironmentsorinponds,andareadaptable bedonebyeitherincreasingtheefficiencyoffeedutilization for several combinations of fish, shrimp, shellfish, sea urchin by animals, or feeding them on cheap or natural resources and seaweeds (Neori etal., 2004; Ren etal., 2012). These thatdonotcompetewithhumanfoodsupply.Strategiesfor systems would decrease some of the inputs needed for pro- inputreductioncanalsodependonthenaturalpreservation duction (e.g. water, nutrients and land) but they are energy ofsupportingservicesingrasslandsorponds. demanding. As pointed out by Martinsetal.(2009), a small Improving the efficiency of nutrient utilization by the waterexchangerateinRAScanalsocreateproblemsresulting animals can help reducing the import of nutrients from from the accumulation of growth-inhibiting factors coming outside the farm. Research initially focused on pigs and from fishes (e.g. cortisol), bacteria (metabolites) and feed poultry,asthesespeciescompetedirectly withhumanfood (metals).Maizehasbeenwidelycultivatedtoproduceforages supply.Lowdigestibilityofphosphorous(P)inpigfeedswas with a high-energy density, but requires large quantities of partly alleviated by the diet supplementation with natural water during summer in temperate areas. Sorghum, with microbial phytase (Dourmad et al., 2009). Benefits of similarnutritionalcharacteristicsbutgreaterresistancetowater improvingtheefficiencyoffeedutilizationcanbeextended stress,couldbeusedforanimalfeeding(Selleetal.,2010). by appropriate feeding practices: in laying hens, sequential Asanalternativetomineralfertilization,plantproduction feeding of wheat grain and protein–mineral concentrate canbestimulatedbytakingadvantageofsynergiesbetween improved feed conversion, and could facilitate the use of plant species. In grassland-based production systems, local feedstuffs introduced as whole grains, thus reducing grass–legume mixtures can achieve high-forage yields as a feedingcosts(Faruketal.,2010).Inorganiceggproduction result of symbiotic nitrogen (N) fixation in legume nodules. systems, stimulating the hens to exercise natural foraging Altering the composition of forage mixtures did not affect behavior reduced the import of nutrients into the system: dry matter intake,milk production or blood metabolite pro- high-producinglayerswereabletoforageoncropsconsist- files of lactating Holstein cows (Soder etal., 2006). Func- ingofgrass/clover,pea/vetch/oats,lupinandquinoawithout tional diversity enhanced the resistance of temperate negative effects on health or performance (egg weight and grasslands to weed invasion in both extensively and inten- BW; Horsted and Hermansen, 2007). Geese that grazed sively managed swards (Frankow-Lindberg et al., 2009). unfertilized grass growing between tree rows in a walnut Including forages in the crop rotation also led to higher plantation increased walnut production by 26% and tree yieldsinthegraincropsplantedaftertheforage,becauseof growthby6%(Duboisetal.,2008).Therewasnomicrobial lesssoildisturbance,increasedsoilorganicmatterandweed contamination (Escherichiacoli) of the fruits if geese were control (Gliessman, 2006). In aquaculture systems, pond removedatleast2monthsbeforeharvesting. productivity can be increased by introducing submerged Feeding systems based on natural resources and agri- substrates in water to naturally stimulate fish productivity. cultural by-products enable to spare resources for human This principle is based on traditional fishing methods used food supply. Permanent pastures and rangelands are cheap in Africa (Acadjas; Bene and Obirih-Opareh, 2009) and 1031 Dumont,Fortun-Lamothe,Jouven,ThomasandTichit Asia (Samarahs and Katha fisheries; Shankar etal., 1998), andlabor)inanintegratedsystemwherehigherfruitquality, wheretheperiphyton–acomplexassemblageofallsessile due to organic fertilization by horse manure, and diversifi- biota attached to the substratum, including associated cation increased farm productivity and led to better eco- detritus and micro-organisms – grows and can constitute a nomic results (Gonza´lez-Garcı´a etal., 2012). In intensively natural food for fishes. Submerged substrates also offer managedwetlandsofsoutheasternAsia,farmersareadding them shelter, while their associated microfauna helps to an aquaculture component to an already integrated crop– improve water quality through the trapping of suspended livestock system. These integrated agriculture–aquaculture solids,organicmatterbreakdownandenhancednitrification. (IAA) systems are based on the recycling of nutrients The control of C:N ratio in-pond water through carbohy- between farm components (Prein, 2002): livestock manure drate addition offers another alternative to enhance micro- and other farm wastes fertilize fish ponds, pond sediments bialdevelopment,proteinrecyclingandbiomassproduction. fertilizecropsandcropco-productsfeedlivestock(Figure1). According to Bosma and Verdegem (2011), manipulating When animals are integrated into agrosystems in this way, C:N ratio doubled protein input efficiency in ponds, while more of the ecosystem processes operating in natural substrate addition enabled a twofold to threefold increase systems can be incorporated into the functioning of the inproduction. system, increasing its stability and sustainability. Excreta fromonespeciescanevenbedirectlyusedascomponentsof Decreasingpollutionbyoptimizingthemetabolicfunctioning formulated diets for another species: for example, West offarmingsystems Africandwarfgoatscouldbesustainedwithpoultryexcreta NandPexcretionandgreenhousegasemissionperanimal for better live-weight gain, feed conversion ratio, carcass can be manipulated through diet (Martin etal., 2010 for yield and better economic returns to the farmers (Alikwe mitigating CH emission in ruminants) or appropriate feed- etal.,2011). 4 ingpractices(phasefeedingforreducing NandPexcretion In RAS, water quality can deteriorate as a result of fish inpigs;Dourmadetal.,2009),butfurtherimprovementscan catabolism and uneaten feed, an effect that is modulated be expected using the agroecology concepts. The main according to fish species, stocking density and feed char- synergyderivedfrommixingcropsandanimalsresultsfrom acteristics. Thus, water becomes enriched in nitrogenous animalmanuresbecomingaresourceinsteadofanuisance, compounds,Panddissolvedorganicmatteranddepletedin because they are rich in nutrients and provide soil micro- dissolved oxygen. Maintaining water quality, despite very organismswithakeysourceofenergy. limited water exchange, requires efficient mechanical and Anintegratedfarmisoneinwhichlivestockareincorpo- biological water treatments. To improve water treatment rated into farm operations specifically to capture positive efficiencybyoptimizingthemetabolicfunctioningoffarming synergiesamongfarmunits(i.e.toperformtasksandsupply systems,somerecentapproachesaimtocombineRASwith services to other farm units) and not just as a marketable anIntegratedMulti-TrophicAquaculture(IMTA).Thisapproach commodity (Gliessman, 2006). Integration of cropping with is based on the cultivation of aquaculture species (principally livestocksystemsallowsbetterregulationofbiogeochemical finfish) with other extractive aquaculture species (principally cycles and environmental fluxes to the atmosphere and seaweeds, and suspension and deposit feeders such as mus- hydrosphere through spatial and temporal interactions sels,oystersandshrimps).Theobjectiveistorecapturesomeof amongdifferentfarmunits.Inself-sufficientlow-inputdairy thenutrientsandenergythatarelostinfinfishmonocultures, farms in Brittany, a part of the arable crops is used for and transforming them into additional crops with commercial homegrown feeds, and grass–legume mixtures are inte- value(Neorietal.,2004;Renetal.,2012). gratedincroprotationwithlegumesallowingareductionin fertilizer inputs (Alard et al., 2002). The longer the ley Enhancingdiversitywithinanimalproductionsystems durationwithinarotation,thegreateristhepotentialforsoil tostrengthentheirresilience organic C sequestration and mitigation of N losses to the Agricultural intensification has drastically reduced diversity, environment (Franzluebbers, 2007). In permanent pastures, that is, the variety of both plant and animal species and grasslanddiversitymayalsoreducerisksofnitrateleaching thevarietyofmanagementpracticesandproductionfactors. becauseofincreasedcomplementaritybetweenspeciesinN Recent empirical evidence suggests that we have under- uptakeandwateruptake(DeDeynetal.,2009).Pigfarming estimated the potential for diversity in animal production systems need to optimize organic N and P recycling and systems (Tichit et al., 2011). Diversity is an essential minimize nutrient leaching. It should be possible to reach property, as it is expected to strengthen the resilience of close to 100% efficiency for P retention in the system. animal production systems through mechanisms operating SystemefficiencyismuchlowerforN(about50%)because atdifferentlevels. of gaseous emissions of NH , N and N O, but it can be At herd level, diversity in both animal species and man- 3 2 2 improved in different ways by reducing gaseous emissions agement practices secures pastoral systems (Mace and fromtheexcreta,improvingcropNfertilization,andinclud- Houston,1989;Tichitetal.,2004).Rearingdifferentanimal inglegumeforagesincroprotations(Rigolotetal.,2010).In species offers a risk-spreading strategy against droughts, Cuba,horsesgrazinggrass–legume mixtures in citrusinter- disease outbreaks and market price fluctuations. Adapting rowsprovidedefficientweedcontrol(savingfuel,herbicides management practices to the biological characteristics of 1032 Ecology-basedalternativesforanimalproduction Livestock Plant production ,,, Feed (crop co-products) Fertilization (manures) (Ruminant, pig poultry…) (Fruit, rice…) Fertilization (manFuereeds) (macrophyte) and water Fertilization C(rpoop nirdr isgeatdiiomn e(ntw)aetrteirli)zation (crop co-products) F Aquaculture in pond Fish of different species (e.g. carp, tilapia…) Figure1 Simplifiedflowdiagramoftheinteractionswithinintegratedagriculture–aquaculturesystems. eachspecies isalsoa keylever to ensureresilience(e.g.by of selective grazing according to breed morphological and modulatingbreedingpracticesaccordingtofemalelongevity physiological traits. In late season, Salers beef cows with a andclimatesensitivity).Combiningseveralherbivorespecies relatively high milk yield potential maintained daily milk at grazing enables higher overall vegetation capture and yield at the expense of body condition, whereas Charolais live-weightgain(NolanandConnolly,1989).Theprincipleof cows,whichhavelessmilkpotentialreducedmilkyieldbut these systems is the use of multiple spatial niches and food lostlessliveweight(Farruggiaetal.,2008).Inagro-pastoral resourcesthatalsoapplyforaquaculture.Indeed,inthepopular systems, the feeding system is based on complementarities rohu(Labeorohita)andcarp(Cyprinuscarpio)combinationin between cultivated grasslands, which are used to secure south Asia, carp browsing the sediment for food oxidize the animal performance in crucial periods such as mating or pondbottomandsuspendnutrientsaccumulatedinsediments, lactation,andrangelands,whicharemostlygrazedattimes leadingtoupto40%higherrohuproductionandalmostdou- when the animals have low nutrient requirements (Jouven blingpondproduction(Rahmanetal.,2006).Withinamono- etal.,2010).Whentheavailabilityoffeedresourcesislowor specific ruminant herd, diversity of lifetime performance is unpredictable,definingseasonalprioritiesbetween animals suggested to act as a buffer by stabilizing overall herd with high requirements or key production objectives (e.g. production. Managing diversity over time becomes a central improving body condition), which will need to be given issueinlargeherdswheremanagementstrategiestargetedat priority access to the best resources, and animals with low different herd segments are expected to increase overall per- requirementsorsecondaryproductionobjectives,alsohelpsin formance (Leeetal., 2009). Diversity in lifetime performance thedesignofefficientfeedingsystems.Thediversityofgrass- emerged from complex interactions between herd manage- landtypeswithinafarmhasbeenshowntoimprovefarmself- mentpracticesandindividualbiologicalresponses(Puilletetal., sufficiency for forage in both dairy (Andrieuetal., 2007) and 2010). These interactions generated contrasting groups of sucklerfarms(Martin,2009).Recentworkhasalsoemphasized females with different production level and feed efficiency. that a diversity of grazing management practices, that is, in The relative size of these groups in the herd was thus a key terms of stocking rate and periods, can enhance ability to determinantofoverallperformance. overcomedroughtevents(Sabatieretal.2012). A diversity of forage resources also helps secure the feeding system against seasonal and long-term climatic Preservingbiologicaldiversityinagroecosystemsby variability. Grazing animals take advantage of resource adaptingmanagementpractices diversity to maintain daily intake (Agreil etal., 2005) and In the past decade, concern over biodiversity erosion has performance(Dumontetal.,2007a),withcontrastingeffects spread to domestic biodiversity (e.g. animal genetic resources 1033 Dumont,Fortun-Lamothe,Jouven,ThomasandTichit andlocalbreeds;Taberletetal.,2011).Higherperformance because both can benefit from a management strategy on of commercial breeds means that local breeds tend to be thebasisofallocatingspecificfunctionstograsslandplotsin replaced by more productive ones, or at least outcrossed. relation to vegetation type. Jouven and Baumont (2008) Lossofgeneticdiversityalsooccursincommercialbreedsvia modeledgrassland-basedbeefsystemsandfoundthatmeat the development of artificial insemination, with only a few production could be maintained by deploying biodiversity- malesbeinginvolvedinreproductionschemes.Althoughthe friendly practices on up to 40% of farm area; the practices narrow differences in diet selection between local and resulting in the optimal production–biodiversity equilibrium commercialbreedsingrassland-basedsystemsmayprevent depended on farming context, that is, type of grassland, any clear management implications being identified overall stocking rate and herd management. Combining (Dumontetal.,2007b),localbreedshavegreaterabilitiesto different management practices (in terms of grazing inten- survive, produce and maintain reproduction levels in harsh sity and cutting frequency) was found to improve produc- environments.Usinglocalbreedsisthuswellsuitedtoeco- tion/biodiversity trade-off, but this improvement was less nomically marginal conditions, owing to reduced veterinary costly for extensive than for intensive farms (Tichit etal., intervention, ease of breeding and lower feedstuff costs. 2011). Benefits of management practice diversity are even Animal products from traditional breeds with strong local greater at landscape scale. Recent work has demonstrated identity can fetch premium prices, as consumers perceive that the proportion of management practices (grazing v. them as being of superior sensory or nutritional quality, or cutting)andtheirspatialarrangementcanaffectthelong-term areattractedbytheimageofaparticularregionortradition dynamics of bird populations in agro-landscapes. Converting (Casabianca and Matassino, 2006); this process could help certainintensivepracticesintoextensiveonesaffectedpro- preserveresistanceoradaptationtraitsthatwouldotherwise duction; however, acting on the spatial arrangement of berapidlylostanddifficulttorescue. practices to increase landscape heterogeneity helped to Agricultural intensification and homogenization are reconcileproductionandbiodiversity(Sabatieretal.,2010). importantdrivingforcesoffloraandfaunadiversityerosion Somelandscapefeaturescanexertmultiplefunctionsand in temperate agroecosystems. At field scale, grassland thus play a role in biodiversity conservation. A typical management for production purposes usually conflicts with exampleisextensivefishponds,whichformfoodproduction grasslandmanagement for conservation purposes(Plantureux ecosystems, attractive landscape features and a habitat for etal.,2005).Biodiversityingrasslandsthustendstoincrease wild bird species. In fishponds with controlled fish biomass as grass utilization decreases (Klimeketal., 2007; Dumont (400kg/ha),thepresenceofaquaticvegetationover10%to etal., 2009), but this compels farmers to underutilize their 15%ofthetotalareaimprovedwaterquality,benefitedfish grasslands, leading to production losses per unit area. This reproduction and offered a refuge and nesting habitat for stresses the need to test for practices able to preserve bio- waders(Bernard,2008).However,theinteractionsbetween diversity while still ensuring good economic returns. Late thebioticandabioticcompartmentsoffishpondsarecomplex, grazing (Sjo¨din, 2007), preserving legume-rich grasslands anddependonpracticesandregionalconditions. (Goulson etal., 2005) and introducing sown margin strips at the edge of arable fields (Marshalletal., 2006), favored Casestudies pollinator abundance and species richness as a result of positivetrophicinteractions.Farruggiaetal.(2012)recently Agroecology implies considering agroecosystems as a showed that temporarily excluding cattle from pastures whole,intheirbiological,technicalandsocialdimensions.It during flowering peak can offer an opportunity to double goesfurtherthan adjustingpracticesincurrentagroecosys- grasslandbutterflypopulationswithoutdecreasingstocking tems; it integrates interactions among all agroecosystem rate. In southern Sweden, Franze´n and Nilsson (2008) con- components and recognizes the complex dynamics of eco- cluded that 20% to 50% of semi-natural farmland left logical processes. We therefore present six case studies ungrazed in May to July to provide abundant nectar, and coveringalonggradientofproductiontypes,intensification pollen resources could compensate for intense grazing levels and biogeographical conditions. They relate to either applied on parts of the remaining farm area. The choice of agroecology or industrial ecology. The first case study is these temporarily ungrazed plots should take into account emblematic of linkages between farming sub-systems; it not only the biodiversity ‘potential’ of each plot, but also mainly concerns Asia and South America, and has not yet their location, so that they can act as dispersal sources or spreadtootherpartsoftheworld.Thesecondandthirdcase ecological corridors (O¨ckinger and Smith, 2007). Manip- studiesillustrategrasslandorrangeland-basedsystemswith ulatingthetimingandintensityofgrazingthroughoutspring eithersheepordairycattle.Althoughourtwoexamplesare is also an alternative management tool for grassland bird French, such systems are found in many parts of the world conservation that does away with recommendations based (United States of America, New Zealand, Australia) where onlategrazingorgrazingexclusion(Durantetal.,2008). they represent sustainable alternatives to large-scale inten- At farm level, maintaining contrasting management sivesystems.Thefourthcasestudyfocusesonrabbitorganic practices is crucial for plant and animal species that share farming;thoughstillmarginal,thissystemisofinterestasit differenthabitatrequirements.Atthisscale,productionand exploresalternativesto confinementandaimstoreconnect conservation objectives are not necessarily in conflict, animal production with the land. The fifth case study deals 1034 Ecology-basedalternativesforanimalproduction Table1Themainagroecologicalprinciplesthatapplyinsixcasestudiesrangingfromgrassland-basedsystemstolarge-scaleintensivesystems Casestudiesinthetext Principle IAAsystems Dairycows Pastoralsheep Organicrabbits Pigs RASfish Integratedmanagementofanimalhealth ** * ** Reduceinputsneededforproduction *** *** ** *** *** ** Reducepollutions ** *** * *** *** Takeadvantageofsystemdiversity ** ** *** ** * Preservebiologicaldiversity * ** * Agroecology X X X X Industrialecology X X IAA5integratedagriculture–aquaculture;RAS5recirculatingaquaculturesystems. ***Majorimportance;**Important;*Marginal. with a pig farming system in which waste management is 300/household in peri-urban areas of Bangladesh (Karim achieved through the principles of industrial ecology. This etal.,2011).Life-cycleassessmenthasbeenusedtoassess kind of system is under development in Northern and Wes- the environmental impact of IAA systems in the Mekong tern Europe, where the negative environmental impacts of Delta (Phong etal., 2011). Energy requirements per kcal industrialized farming are worsened by the spatial aggre- were twice lower in rice-based medium-input fish farming gation of industrial farms. The sixth and last case study is (14.2kJ/kcal) than in the orchard-based low-input fish emblematic of a policy to reduce water use, pollution and farming system (on average 27.1kJ/kcal). On an average, inputsinintensiveaquaculturesystems.Thistechnologywas environmentalimpacts(globalwarmingpotential,landuse, developedduringthelate1980s,mainlyintheNetherlands etc.)were35%to45%lowerperkgoffishproteinthanper andDenmark.Throughthesecasestudies,weexaminehow kg of pig or poultry protein. However, fish grown under ourfiveprinciplescombineineachsystem(Table1),andwe waste-fedconditionscanbecomecontaminatedwithhuman look at system performance and environmental impact on or animal excreta-related pathogens, antibiotics or anti- thebasisofavailableindicators. biotic-resistant bacteria (Sapkotaetal., 2008). Wastewater and excreta can also contain numerous heavy metals and IAAsystems organicchemicals. IAAsystemspromotenutrientlinkagesbetweentwoormore farmingactivities,oneofwhichisaquaculture(Figure1).To Self-sufficientlow-inputdairysystemsinasustainable increasein-pondnutrientsupply,fertilizationpathwaysstart agriculturenetwork fromplantwasteormanureenteringthewater,followedby The basic principle of French RAD (re´seaux d’agriculture decomposition by pond micro-organisms and in-pond durable)dairysystemsistosustainthelevelofaddedvalue growth of natural fish food such as phytoplankton, zoo- derived from dairy production without necessarily maximiz- plankton,benthicorganismsanddetritus.Whilediversifying ingoutputsperanimalorperunitarea(Alardetal.,2002). production, IAA systems also reduce their environmental A key component consists in maximizing the use of grazed impactvianutrientrecycling. herbageattheexpenseofmaizesilageandreducingtheuse IntheMekongDelta,afirstcategoryofIAAisrepresented ofconcentratefeeds.Grasslandscompriseahighproportion by low-input fish farming with intensive fruit production ofgrass–legumemixtures,andgrazingseasonisextendedin (.5t/haperyearoffruitwithfertilizerinput>100kgN/ha summer, autumn and winter. Herd management is tailored peryear)andaminorricefarmingactivity.Aseriesofnarrow toadaptanimalrequirementsto resourcesbygroupingcal- trencheswithintheorchardssupplieswaterforcropirrigation vingperiods. andtoextractnutrient-richmudascropfertilizer.Differentfish In Brittany, RAD farms involved in the ‘low-input fodder species are commonly reared, but with low yields of 0.5 to system’ agri-environmental scheme demonstrated significant 2.0t/ha per year (Nhan etal., 2006; Phong etal., 2010). environmentalimprovements(LeRohellecetal.,2009):totalN Asecondcategoryisdominatedbyriceproductionwithless- pressure(i.e.excreta,mineralandorganicfertilizersandman- intensive fruitproduction (,2t/haper yearwith lowfertili- ure) was 33% lower (121 v.161kg N/ha for conventional zerinput<50kgN/haperyear).Fishproductionisinponds farms).Frequencyindexofpesticideapplicationsdroppedfrom or in rice fields with fish yields between 2 and 10t/ha per 0.66to0.213yearsaftertheschemewasadopted,becauseof year with moderate input of on-farm seasonal nutrient the increase in grassland area and thresholds imposed for resources. Not just fish yield but also livestock growth per- maize and wheat. RAD farms recorded 33% less energy con- formance,biomassproductionrelativetoinputs(Kumaresan sumptionper1000lofmilkthanconventionalfarmsbecauseof etal., 2009) and economic benefits can all be substantially less mineral fertilization and, to a lesser extent, savings on increased. Introducing tilapia into existing integrated farm- concentratefeedsandfuelformechanization.RADdairyfarms ing systems increased gross margins from US$50–150 to hadalowermilksaleandalowerlandareaperworkunitthan 1035 Dumont,Fortun-Lamothe,Jouven,ThomasandTichit conventionalfarms(RAD,2010).Milkquotawascomparablein grazingalsopreserved nativeMediterranean speciesinthis thetwonetworks,butwasnotmetintheRADfarms,wherethe highlydiversevegetationcommunity.Twomajorlimitations priority wastofeedtheherd at lowest cost.Thus,RADfarms to its implementation on wider scales could be, first, the achievedahigheraddedvalue(h57kv.h44kin2009),largely marked seasonality of production, which concentrates explained by their cost-cutting strategy. They also reached workload and is out of line with market requirements, and ahighernetincomeperworkunit(h19kv.h7kin2009).The second, the management of grazing and manure distribu- moderate decrease in productivity (2200l of milk/ha main tion,whichrequiresclosemonitoringofvegetationdynamics fodder area in RAD v.conventional farms) was largely com- andanimalbehaviour. pensated for by overall reduction in input costs (feed costs nearly halved at h68v.h121/1000l milk and lower mechan- Organicrabbitsystems ization expenses at h265/ha). Such low-input dairy systems Organicrabbitproductionsystemsmeetmostagroecological open up new options for existing farming systems, because principles (Figure 2). In north-western France, 1200 organic they display good economic results while limiting pollution rabbitsarecurrentlyproducedeveryyearfrom70femalesin risks.Atwatershedlevel,theexpansionofsuchsystemswould ameat-sheepfarm.Purebredanimalsareraisedoutdoorsin resultinasignificantdecreaseinNfluxes(Moreauetal.,2012). wireandwoodencagesplaced ontheground,which limits Their limited dependence on nonrenewable energy offers a housingrequirements.Cagesaremovedeverydayin3haof potential advantage when faced with higher energy prices, unfertilized permanent grass–clover pastures, which helps buttheycouldbesensitivetoclimatechange,inparticularinter- fight against coccidiosis, the main threat in organic rabbit annualvariabilityingrassgrowth. production(LicoisandMarlier,2008).Therabbits alsohave accesstolocallygrownhay,alfalfa,straw,seedmixturesand Agro-pastoralsheepfarmingsystems pelletsofcommercialorigin.Strawislaidonthetopofcages In pastoral farming systems, performance can be improved to provide dietary fiber and shade on sunny days. Rabbits by organizing the animal production cycle according to for- frequentlysort thedifferent seeds,andthereforetheirrefu- age diversity and seasonal dynamics. In a meat-sheep farm sals are offered to sheep. Antimicrobial agents have only on the dry Larzac plateau, 280 highly prolific rustic ewes beenusedonceinthelast7years.Animalhealthismanaged were reared fully outdoors on 260ha of native vegetation usingessentialoils,garlicextractandcidervinegar(Benguesmia (2t DM/hayear) plus 18ha of fertilized vegetation (4t DM/ etal.,2011).Thissmall-scaleorganicsystemisautonomous, hayear), 10.2ha hay fields and 2.8ha cereals (Mole´nat but much less productive than the conventional system, in etal., 2005). Ewes were first mated at 19 months, and all which prolific, fast-growing hybrid strains are fed complete lambings were concentrated in spring. Thus, the ewes had pelletedfeed(21v.51rabbits/femaleperyear).Bothprolificacy high nutritional requirements in the period of high grass (6v.8weanedrabbits)andgrowthrate(25v.32g/day)were availability on fertilized then on native vegetation. Mating lowerthanintheconventionalsystem.Mortalitywasquitehigh and rebuilding of body reserves in autumn and early (24%v.10%between2weeksandslaughter),raisinganimal winter was secured by grazing regrowths in fertilized plots. welfare issues. In addition, outdoor housing did not satisfy Replacement lambs and nonlactating ewes grazed native internalandexternalbiosecurity,despitethisbeingapriorityfor vegetation,whichwasdividedintopaddockstoensurelong theintegratedmanagementofanimalhealth.Conversely,use periods for vegetation recovery. The system thus benefited oflocalresourcesandgrazingreducedfeedingcosts.Theeco- fromreplacementewe–lambslearningtoexploitrangelands nomic sustainability of the system was reached by on-farm at a young age and mobilized their ability to express com- sales,ascarcasspricewas7.5timeshigher(h12.5v.h1.67/kg) pensatorygrowth. than in conventional systems. This resulted in gross margin Animal productivity was high at 1.8 lambs per female minusfeedingcostsbeing2.5timeshigherthaninconventional older than 1 year. Of the lambs, 20% were sold ‘lean’ at farms (h281v.h110/female per year). This system is strongly weaningandtheremaining80%weresoldfattenedat3to basedonlocalresourcesandindependenttochemicalanti- 4 months. Up to 68% of feed consumed by the flock was biotics to manage animal health. Owing to low structural providedbyrangeland,and93%offlockrequirementswere costs and high sale prices, it enabled one person to live on supplied by feed produced on-farm. Gross profit margin thefarmfromorganicrabbitproduction,despitepooranimal (h97/ewe) was higher than that simultaneously recorded performance. in 18 meat-sheep farms of central France (h58/ewe; M.BenoitandG.Laignel,personalcommunication)because Towardanecologicallysound,efficientpigfarmingsystem ofhighanimalproductivityandverylowsysteminputs.The Most of the environmental impacts of pig farming systems net income (h24.6k/work unit) was also higher than the areassociatedwith theproduction offeedingredients,ani- 18 meat-sheep farm average (h15.0k/work unit). This sys- mal housing and manure storage. A farm in central France tem thus contributed to a sustainable utilization of natural optimizes the metabolic functioning of the system by using resourcesandrequiredlittlenonrenewableenergy(55.8MJ/ manure from 180 sows to produce biogas for heating and, kglambcarcassbasedonlife-cycleassessment)foramod- after treatment, to fertilize 252ha of cereals, oilseeds and eratenetemissionofgreenhousegases(18.8kgeq-CO /kg peas. All the crops are used to produce pig feeds, except 2 carcass). By limiting the riskof shrub encroachment, sheep sunflower,milletandbuckwheat,whicharesold.Adigester 1036 Ecology-basedalternativesforanimalproduction Conventional rabbit system G L G L e ctis G a pr g Wire cages Complete Highly prolific Artificial Antimicrobial n di in confined pelleted hybrid strain insemination agents ee husbandry feed External renewal Semi-intensive Ext. and int. Br reproductive biosecurity rhythm Prophylaxis Genetic Health Housing Feeding Renewal Reproduction managment Organic rabbit system Housing Feeding Genetic Reproduction Prophylaxis Renewal Health managment e Wire Pastured grass Purebred Natural mating Cider vinegar s cti wooden Hay locally Extensive Essential oils pra cages on Whole seeds adapted reproductive Garlic extract g the ground Pellets Self-renewal rhythm Talcum n di e e Br G L G ... Integrated Reduce inputs Reduce and Take Preserve P E management of needed for manage the advantake biological A animal health production excreta of diversity diversity Figure2 Schematicrepresentationofconventionalandorganicrabbitproductionsystems.Major(solidlines)andmoremarginal(dashedlines)contributions toagroecologicalprinciples(AEP)intheorganicsystem(G5gestation;L5lactation). produces 368.000m3 of biogas from liquid and solid pig and 6%), but reproductive performance was slightly lower, manure, as this proves the most effective way to avoid at10.5(v.11.2)weanedpigletsperlitterand86%(v.89%) environmental losses of CH from liquid manure while also fertilityatfirstmating.Mortalitybeforeweaningwasslightly 4 reducingthebiologicalactivityofdrugresidues(Petersenet lower (18% v.>20%) than in conventional farms, which, al., 2007). The biogas produced 880 electric mWh, the together with 75% of feed ingredients for sows, growing annual electricity consumption of 250 houses, and a heat andfinishingpigsbeingproducedonthefarm,ledtobetter production of 847 thermal mWh. The total volume of bio- economicresults.Markedannualvariationsingrossmargin massrecycledeveryyearthroughthedigesterwas5300t,of per sow were strongly buffered by sales of crops produced which84%camefromthefarmviapigmanureandsilageof onthefarm.Thissystembenefitedemployment,as8.5work intercrops. Rapeseed was pressed to extract oil for the units are needed for production, meat processing, on-farm digestermotor,andthepulpwasrecycledbackintothepig sale and waste recycling; however, it also required a major diet.Animalswereraisedinheatedhousing,exploitingheat initialinvestment,asthedigesterinstallationcosth793k,of produced from the digester, thus cutting backenergy costs which55%wasownfunds. andgreenhousegasemission (Rigolotetal.,2010).Sixdif- ferent diets were produced on the farm to meet pig nutri- IntensivefishfarminginRAS tional requirements. Growth performance was similar or Africancatfish(Clariasgariepinus)occupiessecondplacein slightly better than in conventional French pig farms (gain- Dutch fish production, and is produced exclusively in RAS, to-feedratio2.7andmortality4.6%ingrowingpigsv.2.65 which basically consists of two growth phases. The first 1037

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farming systems: agroecology mainly by stimulating natural processes to reduce inputs, and industrial ecology by closing system loops E-mail: [email protected] . alternate grazing with cattle reduces parasite burden in .. estimated the potential for diversity in animal production.
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