Fish Welfare in Aquaponic Systems: Its Relation to Water Quality with an Emphasis on Feed and ...

18 Pages·2016·0.81 MB·English

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Yildiz, Hijran Yavuzcan; Robaina, Lidia; Pirhonen, Juhani; Mente, Elena; Domínguez,
Author(s):
David; Parisi, Giuliana

Title: Fish Welfare in Aquaponic Systems : Its Relation to Water Quality with an Emphasis
on Feed and Faeces : A Review

Year: 2017
Version:

Please cite the original version:
Yildiz, H. Y., Robaina, L., Pirhonen, J., Mente, E., Domínguez, D., & Parisi, G. (2017).

Fish Welfare in Aquaponic Systems : Its Relation to Water Quality with an Emphasis
on Feed and Faeces : A Review. Water, 9(1), Article 13.

https://doi.org/10.3390/w9010013

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water
Review
Fish Welfare in Aquaponic Systems: Its Relation
to Water Quality with an Emphasis on Feed and
Faeces—A Review
HijranYavuzcanYildiz1,*,LidiaRobaina2,JuhaniPirhonen3,ElenaMente4,
DavidDomínguez2andGiulianaParisi5
1 DepartmentofFisheriesandAquaculture,FacultyofAgriculture,UniversityofAnkara,
06110Ankara,Turkey
2 AquacultureResearchGroup,EcoaquaInstitute,UniversityofLasPalmasdeGranCanaria,
MarineScientificTechnologicalPark,Taliarte,35200Telde,GranCanaria,Spain;
[email protected](L.R.);[email protected](D.D.)
3 DepartmentofBiologicalandEnvironmentalScience,UniversityofJyvaskyla,P.O.Box35,
FI-40014Jyvaskyla,Finland;juhani.pirhonen@jyu.fi
4 DepartmentofIchthyologyandAquaticEnvironment,SchoolofAgriculturalSciences,
UniversityofThessaly,FytokoStreet,N.IoniaMagnesia’s,GR38446Volos,Greece;[email protected]
5 DepartmentofAgri-FoodProductionandEnvironmentalSciences—AnimalScienceSection,
UniversityofFirenze,ViadelleCascine5,50144Florence,Italy;giuliana.parisi@unifi.it
* Correspondence:[email protected];Tel.:[phone]
AcademicEditor:M.HaïssamJijakli
Received:30September2016;Accepted:20December2016;Published:1January2017
Abstract: Aquaponicsisthecombinationofaquaculture(fish)andhydroponiccultivationofplants.
Thisreviewexaminesfishwelfareinrelationtorearingwaterquality,fishfeedandfishwasteand
faecestodevelopasustainableaquaponicsystemwheretheco-culturedorganisms,fish,bacteriain
biofiltersandplants,shouldbeconsideredholisticallyinallaquaponicsoperations. Waterquality
parametersaretheprimaryenvironmentalconsiderationforoptimizingaquaponicproductionand
fordirectlyimpactingfishwelfare/healthissuesandplantneeds.Inaquaponicsystems,theuptakeof
nutrientsshouldbemaximisedforthehealthyproductionoftheplantbiomassbutwithoutneglecting
thebestwelfareconditionsforthefishintermsofwaterquality. Measurestoreducetherisksof
the introduction or spread of diseases or infection and to increase biosecurity in aquaponics are
alsoimportant. Inaddition,thepossibleimpactsofallelochemicals,i.e.,chemicalsreleasedbythe
plants,shouldbetakenintoaccount. Moreover,theeffectofdietdigestibility,faecesparticlesize
andsettlingratioonwaterqualityshouldbecarefullyconsidered. Asavailableinformationisvery
limited,researchshouldbeundertakentobetterelucidatetherelationshipbetweenappropriatelevels
ofmineralsneededbyplants,andfishmetabolism,healthandwelfare. Itremainstobeinvestigated
whetherandtowhatextenttheconcentrationsofsuspendedsolidsthatcanbefoundinaquaponic
systems can compromise the health of fish. Water quality, which directly affects fish health and
well-being,isthekeyfactortobeconsideredinallaquaponicsystems.
Keywords: fishwelfare;waterquality;suspendedsolids;micronutrients;aquaponics;sustainability
1. Introduction
Aquaponics, the combined production of fish in recirculated aquaculture systems and
hydroponically grown plants, has gained increased interest over the last several years due to its
sustainability. Aquacultural waste contains nitrogen (in the form of ammonia and nitrate) and
phosphorus (mainly in the form of phosphate), which are essential nutrients for plant growth.
Water2017,9,13;doi:10.3390/w9010013 www.mdpi.com/journal/water
Water2017,9,13 2of17
The plants filter dissolved waste products from the system by utilizing them as a nutrient source,
therebyreducingtheneedforbiologicalorchemicalfiltrationforwaterchangesandwaterquality
management. Theuseofdissolvednutrientsfromfishexcretaforplantproductionhasbeenshownto
increaseplantbiomass,andfreshwateraquaponicsystemscanbeusedtoreducetheenvironmental
effectsassociatedwithfoodproductiononland[1].Aquaponicallygrownproductsprovideconsumers
with high quality, safe and nutritious freshwater fish and plants grown in a sustainable manner.
Asaquaponicsisanintegratedsystemthatcoverstheco-productionofplantsandfish,thecombination
offishandplantsshouldbecompatiblewiththecharacteristicsofeachproductiontypetobalance
nutrientproductionfromfishcultureandnutrientuptakebyplants. Theselectionofplantandfish
speciesbasedonthisfactisofcriticalimportanceintermsofsuitabilityforaquaponicsproduction.
Duetotheircoherentfeatureswithrespecttoaquaponicproduction,tilapia,koi,goldfish,carp,catfish,
barramundi,andvariousornamentalfishspeciesarethemainproducedfishspeciesandthelettuce,
pakchoi,kale,basil,mint,watercress,tomatoes,peppers,cucumbers,beans,peas,squash,broccoli,
cauliflower and cabbage are the main produced plants in the present conditions. In aquaculture
operations,includingaquaponicssystems,fishwelfareisanimportantfactorthatplaysasignificant
roleinasuccessfulbusinessoperation. Fishwelfareingeneralisacomprehensiveissueintegrating
physiological,behaviouralandcognitiveresponses,indicatingadaptiveresponsestostressfulstimuli.
Thus,Segneretal.[2]havestatedthatpoorwelfaremayprovideastrongindicationfortheexistenceof
infectiousandnon-infectiousstressors,leadingtoimpairmentinmaintaininghomeostasis.Fishwelfare
must be viewed as the interaction of multifactorial effects, such as stocking density, diet, feeding
technique,andmanagementprocedures,possiblyaffectingstresslevels,subsequentstresstolerance,
health,andthepresenceofaggressivebehaviour. Ithasbeenrevealedthattheseeffectsarerelated
withthewelfareoffarmedfish. Toimprovethequalityoftheproductwithincreasingitsmarketvalue
andtoachieveapositivepublicperception,weakfishmustbeavoided,andhealthyanimalsmustbe
raisedinaccordancewithwelfarestandards[3].
Fishwelfareinaquaponicsystemscanbeanimportantcriterionfortheconsumer. Theconditions
inaquaponicsystemsshouldpromotefishgrowthandhealth,commonlyregardedasindicatorsof
fishwelfare, todeliverhighqualityproductstoconsumers. Inaddition, itiswellestablishedthat
optimalgrowingconditionsarenecessarytofulfiltheessentialphysiologicalrequirementstopromote
fishhealthandwelfare. However,thestudyoffishwelfareisstilllackingforthespeciesculturedin
aquaponics. Theaimofthispaperistoreviewthepotentialfactorsresultingfromfishnutritionand
waterqualityparametersonfishwell-beingunderaquaponiccultureconditions.
2. WaterQuality
Water quality parameters are of major concern in hazard identification for the welfare risk
assessment of various aquaculture operations; hence, aquaponic systems are not distinct from
aquaculture. Fishraisedinaquaponicsystemsrequiregoodwaterqualityconditionswhichmeanthat
parameterssuchasdissolvedoxygen,carbondioxide,ammonia,nitrate,nitrite,pHmustbewithin
acceptablespecies-specificlimits. Suddenchangesinthefishstockingdensity,growthrate,feeding
rateorwatervolumecanelicitrapidchangesinwaterquality;hence,regularmeasurementofthose
criticalwaterqualityparametersisessential. Thedeteriorationofwaterqualityparametersaffects
fishphysiology,growthrate,andfeedefficiency,leadingtopathologicalchangesandevenmortality
underextremeconditions[4,5]. Intermsofaquaponicsystemsandconsideringthefishwelfareissues,
carryingcapacityisofmajorconcernformaintainingthebalancebetweenplantandfishrequirements
inaco-culturemedium. Carryingcapacityexpressesthemaximumbiomassoffishinthesystemwith
acceptablewaterqualitylimits. Thecarryingcapacityofagivenamountofwaterisdeterminedby
theoxygenconsumptionrateofthefishandtheirresponsestoammonia,CO andotherpotentially
2
toxicmetabolicwastesthatareproduced[5]. Stressinvolvesaseriesofphysiologicalandbehavioural
reactionsthathelpfishresistdeathoradapttochangingconditions.Whenstressissevereorprolonged,
thecapacityofthefishtore-establishhomeostaticnormscanbeinadequate. Theultimateresultmay
Water2017,9,13 3of17
includeimpairedimmunefunctionordeath[6]. Thestressresponsesoffishtoenvironmentalstressors
arecomplex;therefore,evaluatingtheenvironmentalconditionsandunderstandingtheirpotential
deleteriouseffectsonfishareofutmostimportanceinanysystemthatholdsfishincaptivity.
For the welfare of fish in an aquaponic system, water quality is the primary environmental
consideration with a potential to markedly affect fish health. Fish exist in intimate contact with
the water through the huge surface area of the gills and skin, and it is widely acknowledged that
fish are vulnerable to inappropriate water quality. Water provides fish with the oxygen required
tosurvive,dilutesandremovespotentiallytoxicmetabolites,andprovidessupportagainstgravity.
Inappropriatelevelsofwaterqualityparametersaffectphysiology,growthrateandfeedefficiency
(biomassincrease/feedfed)andmaycausenegativestimuli. Fromtheperspectiveofaquaponics,
thestabilizationofthechemicalcompositionofwaternormallyrequiressometimedependingonthe
temperatureandarangeofotherfactorssuchasstockingdensity. Thestabilityofwatercharacteristics
in aquaponic systems may set the biological limits for sustainable production. In other words,
aproductionformatforco-culturedspecies(aquaticorganismsandplants)impairingthebiological
capacityofthefishmaybecausedbyunstablewaterconditions,whichaffectthewelfareconditions
throughcomplexinteractionsbetweenwaterqualityparameters.
Dissolved oxygen (DO) is the primary water quality consideration for aquaponic systems as
in other aquaculture units. Fish extract oxygen from the water by passive diffusion through the
gills. AnadequateconcentrationofDOinthewaterisrequiredtofacilitatepassivediffusiondown
a concentration gradient from the water into the blood [7]. If DO concentrations fall below the
requirementsofthefish,thenfishcannotconvertenergyasefficientlyintoausableform,resulting
inreducedgrowthrate, feedefficiencyandswimmingability[8]. Theimmediateresponseoffish
to decreased DO concentrations is to increase the opercular ventilation rate and show a gasping
response[9].
Inaquaponics,theminimumoxygenlevelstopromotegoodhealthandphysiologicalconditionsin
thefishstockcanchangebasedonfishspeciesandfishsize.Thesolubilityofoxygeninwaterdecreases
asthetemperatureincreases. ColtandTomasso[7]contributedthebasicpointsinaquaculturepractise
thatareofimportanceinaquaponicsystemswhenconsideringtheallowableDOlevels,i.e.,
• elevatedtemperatureincreasesthemetabolism,respirationandoxygendemandoffish;
• fish increase their oxygen uptake after feeding due to the oxygen demand required for feed
processing,calledspecificdynamicaction;
• oxygenconsumptionisproportionaltothesizeandnumberoffishinagivensystem;
• smallerfishusemoreoxygenperunitweightthanlargerfish;
• stressful conditions such as impaired gill function, exposure to stressors and decrease in
oxygen-carryingcapacityleadtotheincreaseinoxygendemandoffish.
Ingeneral,therecommendedlimitforDOlevelsinfishcultureis6ppmforcoldwaterfishand
4ppmforwarmwaterfishtoprotectthehealth[9].
In aquaponics, the nitrogen cycle is a critical factor. The cycle begins with the introduction
of protein in fish feed, which is ingested by fish and then excreted to the aqueous phase in the
form of total ammonia nitrogen (TAN, i.e., NH and NH ). Ammonia is first oxidized to nitrite
3 4
(NO )byammonia-oxidizingbacteria(mainlyNitrosomonasspp.) inabiofilterandthenconverted
2
tonitrate(NO )bynitrite-oxidizingbacteria(mainlyNitrobacterspp.). Intheaquaticenvironment,
3
ammoniaexistsintwoformsinequilibrium: un-ionisedammoniaandionisedammonium. Thus,
thetotalammoniaconcentrationisthesumoftheconcentrationsofun-ionisedammoniaandionised
ammonium. TheequilibriumbetweentheNH andNH + variesinrelationtothevariousfactors,
3 4
mostsignificantlytheconcentrationofhydrogenions(i.e.,pH)andtemperature.
Inanaquaponicsystem,mostoftheammoniafoundinafishfarmisproducedbythefishasin
aquaculturesystems. Ammoniaistheprimarywastemetaboliteproducedbyfishfromthecatabolism
ofproteincontainedwithinthefeed.Mostbiologicalmembranesarepermeabletoun-ionisedammonia
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and relatively impermeable to ionised ammonium. Therefore, in fish, ammonia in the external
environmenteitherinducesretentionofendogenousammoniainthefishorentersviathegillsby
passive diffusion down a concentration gradient. The ammonia is excreted from the fish via the
gills[10].AmmoniatoxicityisdependentprimarilyontheconcentrationofammoniaandthepHofthe
environment. RandallandTsui[11]reportedthatacuteammoniatoxicityaffectsthecentralnervous
system of fish and manifests as a neurological disorder. Ammonia interferes with physiological
processesthateventuallyresultinthedeathofcellsinthebrain;however,ammoniatoxicityandits
exactnaturearenotunderstoodinfish. Highconcentrationsofammoniadecreasesurvival,inhibit
growth,andcauseavarietyofphysiologicaldysfunctions. Thehighlevelofammoniainwateracts
asastressorinthatitstimulatesthereleaseofcorticosteroidhormonesintocirculation,affectingthe
welfareofthefish. Masseretal.[12]statedthatun-ionizedammonianitrogenconcentrationsaslowas
0.02–0.07ppmhavebeenshowntoslowgrowthandcausetissuedamageinseveralspeciesofwarm
waterfish. However,tilapiatoleratehighun-ionizedammoniaconcentrationsandseldomdisplay
toxiceffectsinwell-bufferedrecirculatingsystems. However, insensitivespeciessuchasrainbow
trout(Oncorhynchusmykiss),therecommendedlevelofun-ionisedammoniais<0.02mg·L−1[9]. Inthe
management of recirculating systems, ammonia should be monitored daily. If the total ammonia
concentrationsstarttoincrease,thebiofiltermaynotbeworkingproperlyorthefeedingrate/ammonia
nitrogenproductionishigherthanthedesigncapacityofthebiofilter.
Nitritebecomestoxicevenatlowconcentrationsformanyfishspecies[13]. Thedegreeoftoxicity
to nitrite varies with species. In freshwater fish, nitrite enters through the gills. Nitrite ions are
actively taken up through the chloride cells, and they can be pumped in against a concentration
gradient[14]. Bloodplasmaconcentrationsofnitritecanaccumulateuptotentimesgreaterthanthe
ambientwaterconcentration[15]. Infish,bloodisthemaintargetofnitriteaction. Nitritediffuses
from the blood plasma into red blood cells, where it oxidises the Fe2+ in haemoglobin (Hb) to the
Fe3+oxidationstate,convertinghaemoglobinintomethaemoglobin(metHb). MetHbreducesthetotal
oxygen-carryingcapacityoftheblood[16]. Nitriteexposureresultedinareductioninhaemoglobin
andhaematocritintilapia(Oreochromisniloticus)withmildmethaemoglobinaemiafollowingexposure
to0.50and1.38mg·L−1 NO −-Nfor48-hstatictests[17]. Nitriteexposureintherangeof0.50and
2
1.38mg·L−1NO −-Ncausedanincreaseinmethaemoglobinlevels. Methaemoglobinconcentrations
2
in excess of 50% are considered threatening to fish [18]. The physiological disturbances may be
primarily rooted in the hypoxia caused by methaemoglobin accumulation. Thus, it is predictable
thattheoxygenstarvationinduceshyperventilation. Becausethegillsaredirectlyincontactwiththe
aquatichabitat,themorphologicalandphysiologicalalterationsinthegilltissueareofmajorconcern.
Svobodovaetal.[19]reportedthathyperplasia,vacuolisationandelevatednumbersofchloridecells
werethemainhistologicallesionsthatoccurredinthegillsofnitrite-treatedcarp(Cyprinuscarpio).
Nitritecanreachhighconcentrationsinrecirculatingaquaculturesystemsinwhichhighdensitiesof
fisharekept. Scaledfishspeciesaregenerallymoretoleranttohighnitriteconcentrationsthanspecies
suchascatfish,whichareverysensitivetonitrite[12]. Lowconcentrationsofdissolvedoxygenaffect
thetoxicityofnitrite. Becausenitriteaffectstheabilityofbloodtotransportoxygen,areductionin
ambientwaterDOconcentrationsincreasestheeffectoftoxicity. Althoughtherearemanystudies
aboutacuteandsublethaleffectsofnitriteonfishintheliterature[14,16,20–22],comprehensivestudies
onthechroniceffectsofnitriteondifferentfishspeciesunderaquaponicconditionswillbenecessary
consideringtheinteractionofplantrootsandtheefficiencyofrelatedbacteriainthesystem. Inbrief,
therelatedbacteriathatmaybeinvolvedinaquaponicsystemsarethefollowing: ammonia-oxidizing
bacteria(AOB),includingbacteriaofthegeneraNitrosomonas,Nitrosococcus,Nitrosospira,Nitrosolobus,
andNitrosovibrio,andnitrite-oxidizingbacteria(NOB),includingbacteriaofthegeneraNitrobacter,
Nitrococcus,Nitrospira,andNitrospina[23].
In general, information on chronic nitrate toxicity in cultured fish species across various life
stages is limited. Nitrate, the end product of nitrification, is relatively non-toxic except at very
highconcentrations(over300ppm[12]). However, Davidsonetal.[24]reportedthatcaseswhere
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recirculatingaquaculturesystems(RAS)wereoperatedwithverylowwaterexchangenitratecaused
chronictoxicitytovariousfishspecies.Thus,thestudyofDavidsonetal.[24]underlineshowrelatively
lownitratelevels(80–100mg·L−1NO -N)wererelatedtochronichealthissuesinandwelfareimpacts
3
tojuvenilerainbowtroutunderRASconditions. Changesinswimmingbehaviour,slightlydecreased
survivalandreducedtotalbiomasswerethemainfindingsofimpairedwelfareconditionsinaRAS
system with rainbow trout. Nevertheless, in the case of aquaponics, nitrogen compounds should
alwaysbeevaluatedwiththevegetationfactor. Nitrateandammoniumarethemostcommonformsof
nitrogentakenupbytheplants. Theremovalofnutrientsisaffectedbytheplantspeciesandcropping
method,asreportedbyBuzbyandLin[25]. Thepotentialadverseeffectsofammoniumornitrateon
thefishwell-beingareexpectedtoberelievedwiththeremovalofthesecompoundsviaplantuptake
intheaquaponicsystem. However,thedesigningofaquaponicsystemsandthetechniquesusedare
thefactorsaffectingnitrogencompoundsconcentrationsinthesystemandtheirpossiblestresseffects
onfishaswellasstresstype.
A disruption of the balance between fish, filters and plants at any time may also result in
ammonia or nitrite that could be fatal to the fish and certainly reduce performance and increase
thesusceptibilitytodiseases. Suchdisruptionsmayarisefromasignificantdecreaseinplantorfish
biomass,asignificantincreaseinfeedinput,adecreaseinfiltercapacityasaresultofsloughingof
accumulatedbacteria/organicmatter,acleaningofthesystem,orasuddenchangeinpH.Temperature
isavitallyimportantphysicalpropertyofthewaterinaquaponicsystems. Theamountofdissolved
oxygenisdirectlylinkedwithwatertemperature. Watertemperatureaffectstherateofdecomposition
andphotosynthesis,whichwillaffecttheoxygendemandinsystemsandtheionisationofammonia[7].
Optimal temperatures for growth and spawning have been examined for many species that are
important to aquaponics. Increasing the temperature has been found to increase the growth and
infectiousnessofmanyfishpathogens[4]aswellasthetoxicityofmanydissolvedcontaminants[9].
Allofthesefactorshavethecapacitytocompromisethehealthoffishunderaquaponicconditions.
Modelstudiesonwatertemperaturetomaintainthewell-beingoffisharenecessarytoachieveoptimal
plantgrowthinaquaponicsystems.
ThemanagementofpHisalsonecessaryinaquaponicsystemsbecausepHwillsteadilydecline
asaresultofthenitrificationprocess,whichincreasesH+ andNO − ionsinthesystem. Acrucial
3
iteminaquaponicsystemsispHstabilizationbecauseitiscriticaltoalllivingorganismswithina
cyclingsystemthatincludesfish,plantsandbacteria. MostplantsrequireapHvaluebetween5.5
and 6.5 to enhance the uptake of nutrients. However, the optimal pH of three major bacteria has
beenstatedas(1)Nitrobacter: 7.5;(2)Nitrosomonas: 7.0–7.5;and(3)Nitrospira: 8.0–8.3[26]. However,
intermsofthetoleranceoffishtopHchangesbasedonfishspeciesandsize,therecommendedpH
foraquacultureis6.5–8.5[27]. InintegratingthehydroponicsystemswithaquaculturethepHvalue
seemstobethedrasticfactorinordertoconcurrentmaintenanceofnutrientuptakebytheplantand
optimalpHvalueforfishandthebacteriainbiofilter. pHvalueshigherthan7.0causesthereduced
micronutrient and phosphorus solubility and plant uptake of certain nutrients is restricted in the
aquaponicenvironment[28]. Ontheotherhand,asacidicwaterisoneofthestressorsinaquaculture
environments,lowlevelsofwaterpHinaquaponicsystemshavethepotentialtoaffectnegativelythe
welfareoffish. AnothersubjectrelatedwithpHlevelsistheinteractionbetweenpHandphosphorus
(P)availabilityandspeciation. CeroziandFitzsimmons[29]reportedthatPavailabilitydecreased
withhighpHvalueofaquaponicnutrientsolutionsandinsolublecalciumphosphatespeciesformed.
HencehighpHlevelseemstobeapreclusionintheplantuptakeofPinaquaponics. Intermsoffish
welfare,Pinaquacultureisnotclassifiedasawaterqualityparameterthathasthepotentialtoimpact
onfishhealth/welfare. Itisknownthatphosphoruscanbetoxic,buttoxicityoccursrarelyinnature
andisgenerallynotaconcernexceptfortheindirecteffectsofphosphorus.
It is always important to consider that sustainable aquaponic production requires balancing
nutrient concentrations and pH for the optimal growth of three organisms: plants, fish, and
nitrifyingbacteria.
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Theprimarysourceofcarbondioxideisfishmetabolisminaquaculture. Itisknownthatfree
carbon dioxide is toxic to fish. Fish cannot release endogenous carbon dioxide into water when
ambientCO concentrationsarehigh,resultinginCO increasesintheblood,aconditiondescribedas
2 2
hypercarbia. DuetodecreasesinbloodpHalongwithacidosisinhypercarbia,theoxygen-carrying
capacity of the blood declines (the Bohr effect). Carbon dioxide toxicity can be characterized by
moribundfish, gapingmouthsandbrightredgilllamellae[30]. ThelinkbetweenCO andwater
2
hardness was reported as the cause of nephrocalcinosis in rainbow trout, with the symptoms of
the calcifying material manifesting in the ureters and kidney and as impaired food conversion
efficiency [31]. Land-based, recirculating aquaculture systems as well as aquaponic systems can
exposefishtohigher-than-naturallevelsofaquatichypercarbia. Oxygenisartificiallysuppliedtothese
systemstoincreasefishproduction;however,anincreaseinbiomassnormallyleadstoanincreasein
CO production.
2
Ingeneral, thetolerablewaterqualityparametersforfisharewithinthesamerangewiththe
plantsexceptwatertemperatureandpHintheaquaponicsystem(Table1). Whenconsideringthe
well-beingoffishspeciesinaquaponicsystems,fishspecieswithahightolerancetopHandwater
temperatureshouldbetakenintoaccount. ItisobviousthatpHandtemperaturearetheparameters
thathaveanimpactonoptimizationofaquaponicproductionbothforfishwelfare/healthissuesand
forplantneeds.
Table1.Generalwaterqualitytolerancesforfish(warmorcoldwater),hydroponicplantsandnitrifying
bacteria(fromSomervilleetal.[32]).
Temperature Ammonia Nitrite Nitrate DissolvedOxygen
OrganismType (◦C) pH (ppm) (ppm) (ppm) (ppm)
Warmwaterfishes 22–32 6–8.5 <3 <1 <400 4–6
Coldwaterfishes 10–18 6–8.5 <1 <0.1 <400 6–8
Plants 16–30 5.5–7.5 <30 <1 - >3
Bacteria 14–34 6–8.5 <3 <1 - 4–8
Inaquaponicsystems,specialcareshouldbetakenwhentreatingthefishtoeradicatediseasesor
parasites. Somechemicalsinanaquaponicenvironmentwillharmordestroytheplants,anditiswell
knownthatmanychemicalsandmetalswillalsobeabsorbedbytheplants[33,34],hinderingtheiruse
forconsumption. Theuseofantibioticsfortreatingbacterialinfectionsisoneoption,buttheymay
beabsorbedbytheplants[35],thuscausingwithdrawalperiodsandmarketingproblems;thissame
problemisalsoseenwiththefish.
Inaquaponicsystems,specialcareshouldbetakenwhentreatingthefishtoeradicatediseases,
parasites or water mould. For example, formalin is a common chemical used to treat certain fish
parasitesandwatermould,anditcanalsobeusedinrecirculationsystemsrelativelysafelywithout
compromisingnitrificationinthebiofilter[36]. However,inanaquaponicsystem,formalincanbe
expected to cause severe damage to the plants as formalin added into the soil has been shown to
drasticallydecreaseplantcoverandshootdryweight[37].
Inanaquaponicsystem, theplantsmayalsoinducesomedirecteffectsonthefish, atleastin
theory. Plantsareknowntoproducechemicalsthattheyexcrete,e.g.,throughtheirroots[38],inorder
tomaketheirenvironmentmorefavourabletothemselves. Thisphenomenoniscalledallelopathy,
whichveryoftenreferstothedetrimentaleffectsofplantsinthesurroundingenvironment. However,
theeffectscouldbepositiveaswelldependingontheinteractingorganismsandtheconcentrationof
thechemicalinquestion[39,40]. Allelopathicplants,i.e.,plantsthatreleaseallelochemicals,havebeen
discoveredinseveralphyla[33]. Theconcentrationofallelochemicalsreleasedbyaplantcanalso
varywidelydependingonthesurroundingplantspecies[38],andthiscouldpotentiallycausefish
welfareproblemsinanaquaponicsystemiftheplantspeciesusedproducechemicalstofighteach
Water2017,9,13 7of17
other. However,tothebestofourknowledge,negativeeffectsofpotentialallelochemicalsexcretedby
aquaponicallygrownplantsonfishhavenotbeenreported.
Ontheotherhand,conditionsinhydroponicsystems,andnaturallyinaquaponicsystemsas
well,areoftenperfectforthegrowthofdifferentkindsofalgae[41]. Itisknownthatalsoalgaecan
releaseallelochemicalswhichcanbeharmfulnotonlyforthefishbutalsoforthemicrobiotaandthe
plants[42],e.g.,cyanobacteria(blue-greenalgae)canexcretecyanotoxins,whichcandirectlyplace
fishhealthatrisk,orthephysicalpresenceofthesealgaecanharmthegills[43]. Inaddition,thealgal
spikesofdiatoms(e.g.,Chaetocerossp.) havebeenreportedtodamagethegillsataconcentrationof
fiveorganismspermlwiththeconsequenceofexcessproductionofmucusandinhibitionofoxygen
uptake[44]. Despitethepotentialadverseeffectsofalgaeonfishwehavenotfoundreportedevidence
ofsuchincidencesinaquaponicsystems.
Measures to reduce the risks of the introduction or spread of infection and to reduce the
conditionsenhancingsusceptibilitytoinfectionsarecalledbiosecurity[45].Thesemeasuresshouldbe
ofutmostimportanceineveryaquaponicoperation. Themethodsforincreasingbiosecurityinclude
considerationssuchasthewatersource,sourcesoffishandeggs,preventativedisinfectionpractices
forstaffandvisitorsandthequarantineofnewarrivalsasreportedbyTimmonsandEbeling[45].
3. FeedsandMicronutrients
Thedietanditsuseforthefishrepresentthehighestimpactonthecarryingcapacityofaquaponic
systems[46].Currently,verylittleisknownaboutspecificfishdietsforaquaponicculture;thus,current
dietsforaquaculture,mainlythoseforRAScultureconditions,arewidelyusedforbothpurposes.
Apartfromanadequatenitrogen/energybalanceandacorrectcombinationoffeedingredientsand
particlesize,thedietformulationforaquaponicsshouldcontainadequateimmuno-ingredientsor
additivesthatpromotethebestwelfareconditionstothefishduringthegrowingcycle,thusavoiding
anyextratreatmentsintothesystem. Moreover,theeffectsofspecificfeedsonwaterqualitythrough
diet digestibility, faeces particle size and settling ratio are also important aspects. Water quality
modificationsfromspecificdietsandselectedfeedingstrategieshavebeenrelatedtofishbehavioural
changes [40], which are essential for fish nutritionists to interpret dietary effects on the system.
Food-anticipatoryactivitycanbeagoodwelfareindicator[47],whichmaybeusedinformulafeed
studies. Animportantfactortostudyunderaquaponiccultureconditionswouldbetherelationship
betweenthewholefishexcretaandtheplantnutrientrequirements. Aquaponicstudiesmayimplicate
interdisciplinaryresearchareastoachievemoreadequatefishfeedformulationsandfeedingstrategies,
notonlyfocusingonfishgrowthandwell-being,butalsopromotingthebestplantgrowthandquality
fortheconsumers.
Although the running of an aquaponic system could be improved through optimal fish and
plantspeciesselection[46],andthecorrectfishfeedregime[48],mostofthereportedresearchshows
extra nutrient inputs needed for the plants, which should be added to the growing medium or as
a foliar spray to improve plant growth [49,50]. Although from literature N, Mg and some other
plantnutrientsappeartobeadequatefromfishexcreta,thisisnotthecaseforP,K,Cu,Fe,Mn,Zn
andS[51,52],whicharenormallyincludedinthegrowingbedtobeabsorbedfortheplants. Inthis
senseitisimportanttonotethatnoinformationhasbeenreportedregardingthepossibleimpactof
thesurroundingwaternutrientsonfishwellbeingorwelfare. Itiswellknownthatfishexpendenergy
torespondtothechangesinsurroundingmediumosmolalitybyregulatingtheirbodyfluidvolume
andsoluteconcentrationthroughendocrinecontrol,withmarineandfreshwateranimalsexhibiting
differentstrategiestomaintaintheirhomeostasis(ionicandosmoticgradientsbetweenthebodyfluids
andsurroundingseawater)[53].
Nutritionandfeedinginfluencefishgrowth,welfareandhealthandtheirresponsetophysiological
andenvironmentalstressorsandpathogens. ThemicronutrientsP,K,Cu,Fe,Mn,ZnandSrepresent
a very small percentage in fish feed, and information related to the requirements and effects of
thesemicronutrientsonfishaquacultureisrelativelyscarce. Frompublishedpapers,micronutrient
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deficienciesaremoreextensivelyreportedcomparedwithstudieswhereexcessamountshavebeen
tested, i.e., possible toxicity effects. During last years, the effects of dietary Cu, Mn, Fe and Zn,
importantmicronutrientsinfishmetabolism,haveattractedinterestduetotheirlimitedavailabilityin
plantproteinformulatedfeedsrespecttothehigherfishmealdiets.
Copper (Cu) is an essential metal involved in several Cu-dependent enzymes, which
mostly intervene in the defence against oxidation reactions and include the Cu/Zn superoxide
dismutase (CuZnSOD), but Cu also participates in the production of energy at the cellular level,
inneurotransmission,collagensynthesisandmelaninproduction[54]. LowCulevelsmaygenerate
a reduction in feed efficiency and growth [55], while Cu toxicity produces gill damage and liver
andkidneynecrosis[54,56]. Iron(Fe)isinvolvedinelectrontransport,oxygentransferandcellular
respiration,withaspecialimportanceinhaemoglobin[56,57]. Fecanbepartiallyabsorbedviathe
gills;however,themajorityisabsorbedintheintestine. Fedeficiencycausesanaemia,lowhaematocrit
andreducedFeinplasma,whereasexcessuptakeofFecausesreducedgrowth,poorfeedutilization,
mortalityanddiarrhoea[54,56]. Manganese(Mn)isatransitionmetalessentialforlife,actingasa
cofactorforessentialmetalloenzymesinvolvedinthedevelopmentoftheorganicmatrixofbone[58].
Mnsuperoxidedismutase(MnSOD)intervenesinpreventingtheinitiationoftheradicalchainreaction
whenanoxidationreactionoccurs. MndeficiencyreducesMnSODactivityinfishtissuesandthelevel
ofMn,CaandNainthevertebrae[59]. ExcessMnmayaffecttheintegrityofintestinalimmunity[60],
whichisessentialmostlyinmarinefishtomaintaincorrectionregulation. Zinc(Zn)isanessential
cofactorforseveralmetabolicprocessesinfishandformspartofupto20metalloenzymesimplicated
inlipid,carbohydrateandproteinmetabolism. Znisessentialforstructuralcomponentssuchasbone,
skinandscales;playsanimportantroleinregulatingoxidativestressandimmunity;andintervenesin
reproductiveprocesses. Znisinvolvedinboneformationandmineralizationbyactivatingosteoblastic
cellsandinhibitingosteoclasticboneresorption[61]. Thus,Zndeficiencyinfishcausesslowergrowth
rates, cataracts, skin and fin erosion, and dwarfism [56]. Zinc can be absorbed via the gills and
gut [62–64]. However, the presence of chelators or competitive substances may interact with zinc
absorption. Calcium,phosphates,highwatersalinityandacidicpHaresomeofthefactorsthatcan
alterzincavailability. Zincdeficiencymaythusreduceproductionoverthewholelifecycle[54,56,65].
However, zinc toxicity has scarcely been studied, and most trials only reflect data concerning the
survivalinfreshwaterspeciesexposedtohighlevelsofwaterbornezinc. Probablythemostimportant
toxiceffectofzincisrelatedtotheinhibitionofcalciumabsorption. Calciumandzincsharetransport
channels,andathighlevelsofzinc,calciumuptakeisseverelyreduced[66–69].
As a summary, it is important to note that in aquaculture, fish mineral requirements are still
poorlyreported,withaverylowamountofinformationwithrespecttodietarymineralunbalanceand
excessonfishwelfare. Asfishmayobtainmineralsbothfromsurroundingwateranddiets,research
effortsshouldbemadetounderstandthesharedwaterbornemicronutrientcompatibilityandmutual
benefitsbetweenplantsandfish,andalsotostudytheeffectsofhigherdietarylevelsofthetarget
plantmineralsinthewholeaquaponicproductioncycle,fish,andplants.
4. WastesandFaeces
Allmaterialswhichhavebeenusedbutarenotremovedfromtheaquaculturalsystemduring
harvestingcanberegardedaswaste[70]. Thecompoundscontainedinthefeedaredigested,absorbed
andutilizedinthemetabolicprocessesandretainedindifferentmeasuresinthebodyoffish. Onepart
ofthosecompoundsisexcretedthroughthegillsorasfaeces. Onlyapproximately1/3ofthenutrients
inthefeedareremovedintheharvestofthefishand2/3voidedbyfishduringgrowth[71].
Uneaten feed, excreta, chemicals and therapeutics are retained in the waste produced by
aquaculture.Wasteoriginatingfromthefeedincludesdissolvedcomponents(suchasphosphorus-and
nitrogen-basednutrients)andsuspendedsolids[72]. Fishfoodandfaecesareknowntobethemain
solidwasteinintensiveaquaculture. Thefaecalwastecanbecalculatedbytheproximatecomposition
(reportedonfeedbaglabels)andbytheassociatedvaluesofdigestibility;indeed,theoverallfraction
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offaecesproducedperunitoffeedconsumedisobtainedbysummingtheamountofallindigestible
dietarycomponents.
Theproductionoffeedwastessuchasdustanduneatenfoodhasbeenestimatedtobe20%[73],
whereasotherauthors[74,75]haveproposedarangeof10%to30%ofwasterepresentedbyuneaten
foodalonefromintensiveaquaculture. Throughameta-analysisofpublisheddatafromcommercial
producersinBrazilonexpectedfeedintake,feedefficiencyandotheranimalproductionindicesand
thebodycompositionoftilapia(O.niloticus),NetoandOstrensky[76]estimatedthat18%ofthefeed
given to the animals is not consumed and is lost in the aquatic environment and accumulated in
thesludge.
According to Reid et al. [77], in the case of a common salmon feed, approximately 15% of
consumedfeedbecomesdryfaecalmatter,whileButzandVens-Cappell[78]affirmedthatthefaecal
inputis260gperkgoffoodonadryweightbasis.
Themainphosphoruslossinfishisthroughfaeces. Highphosphoruslossthroughfaeceswasalso
foundbyPettersson[79]inrainbowtroutandbyJohnsenetal.[80]inAtlanticsalmon(Salmosalar).
Hakanson et al. [81] calculated that of the total phosphorus and nitrogen fed to fish, 70% of the
phosphorus and 15% of the nitrogen is lost through faeces, whereas Kristiansen and Hessen [82]
reported loss values of 4.0% for phosphorus and 2.3% for nitrogen in Atlantic salmon, and 3.5%
for phosphorus and 4.1% for nitrogen in noble crayfish (Astacus astacus) faeces. In a recent paper,
NetoandOstrensky[76]proposedthat17%ofthefeedinputfornitrogenand37%forphosphorus
is lost as nutrients from the faeces in Nile tilapia reared in cages. Although the data of Neto and
Ostrensky[76]werebasedoncagebreedingsystems, recentlyGoddeketal.[26]observedsimilar
valuesinRAS.Certainly,thespeciesaffectstheentityoftheselosses,whichareaffectedalsobythe
physiological stage within the species. Neto and Ostrensky [76] also found relevant variations in
feedinglossesinrelationtotheageoftilapia—30.9%forfry,17.0%forjuveniles,17.6%forthegrowing
phaseand16.7%attheslaughterstage.
Over the last several years, the progress in fish nutrition research and in feed manufacturing
for the most important aquacultured species has contributed to a significant reduction of waste.
Theimprovedbio-availabilityofphosphorusandproteinsinthedietshassignificantlyreducedthe
faecalsolidsproducedandimprovedthefeedefficiency[70]. Theadditionofdigestibilityenhancers
inthefeed,suchasphytase,hasimprovedusabilityofphosphorusfromplantproteinsforfishandhas
helpedtoreducethelossofnutrientsaswaste[83].
Thelabileformofphosphorusinthefaeces,aformreadilyavailabletoplantsfortheirgrowth[78],
rangesfrom15%to54%[79,84]. ThequantityofPreleasedbysolidwastesislargelydependenton
temperature(25◦C>20◦C)andpH(higherathigherpHvalues)[84].
Forthereductionofsolidwaste,theimportanceoffeedprocessingandproductionshouldnotbe
underestimated. Feedmanufacturingprocessesaimtoimprovethenutritionalqualityofthedietsbut
alsotoimprovethestabilityandintegrityofpellets,consequentlyreducingthepelletbreakdownin
waterbeforeconsumptionbythefish.
Throughthisdoubleapproach(dietformulationandfeedmanufacturing),feedingmanagement
practiceshavemaximizedthefeedutilizationbyfishand,atthesametime,minimizedtheuneaten
quantity of feed, achieving a more economical process because the economy and efficiency of the
productionprocessarestrictlyconnected[85,86].
Theparticlesizeaffectstheratioofsettleabletosuspendedsolids[77]. Largerparticlesareless
numerousbutoccupyalargervolume,whereassmallerparticlesaremorenumerousbutoccupyless
volumeoverall. Buryniuketal.[87]foundastrictcorrelationbetweenfishsizeandthefaecalsize
classes: faecesfrom1kgAtlanticsalmonwerenotcapturedonmeshopeningsover4mm,whilesome
10%–20%offaecesfrom5kgsalmoncouldbecapturedona25mmmesh. Variabilityinfaecalparticle
sizesispositivelycorrelatedwithfishsize[87,88]. Magilletal.[89]foundthemeansizeofparticles
ofseabream(Pagrusmajor)andseabass(Dicentrarchuslabrax)fedthesamediettorangefrom0.3
to2.5mm(1.4mmmean)andfrom0.3to6.2mm(1.12mmmean),respectively. Fishsizeandspecies