Control of waterborne microbes in irrigation: A review · 2016. 2. 6. · Algae and equipment-clogging bioﬁlms also result from high microbial levels in irrigation water. The lit-erature

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Agricultural Water Management 143 (2014) 9–28

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ontrol of waterborne microbes in irrigation: A review

osa E. Raudalesa, Jennifer L. Parkeb, Charles L. Guyc, Paul R. Fisherc,∗

Department of Plant Science and Landscape Architecture, University of Connecticut, 1376 Storrs Road, Storrs, CT 06269-4067, USADepartment of Botany and Plant Pathology, Oregon State University, 2082 Cordley Hall, Corvallis, OR 97331, USAEnvironmental Horticulture Department, University of Florida, 1549 Fifield Hall, Gainesville, FL 3261, USA

r t i c l e i n f o

rticle history:eceived 19 February 2014ccepted 14 June 2014

eywords:lgaeiofilmhlorinationlant pathogensanitationater treatment

a b s t r a c t

A wide range of plant pathogens have been identified in irrigation water sources and distribution systems.Algae and equipment-clogging biofilms also result from high microbial levels in irrigation water. The lit-erature was reviewed on the effectiveness of water treatment options to control waterborne microbes.Water treatments included chemicals (chlorine, bromine, chlorine dioxide, ionized copper, copper salts,ionized silver, ozone, hydrogen peroxide, and peroxyacetic acid), non-chemical or physical treatments(filtration, heat, and ultraviolet radiation) and ecological alternatives (constructed wetlands, biosurfac-tants, and slow sand filtration). The objective was to summarize the effective dose for controlling targetwaterborne microorganisms. The effective dose for chemical water treatments to control plant pathogenswas in some cases above documented phytotoxicity thresholds, and for most crops and technologiesthe phytotoxicity thresholds remain unknown. Most efficacy research has been conducted on chlorine(20 articles) or copper (18), but only 0–7 articles were found on other water treatments currently in
use, indicating major knowledge gaps in treatment efficacy. Research is needed on control methodsfor algae and biofilms, in vivo pathogen studies, phytotoxicity thresholds, and the relationship betweenpathogen inoculum level and disease incidence in irrigation water. Finally, improved overall systemdesign is required for risk management of waterborne microbes in irrigation, including a multiple barrier approach incorporating pre-filtration, multiple treatment stages, and monitoring of water quality.
Published by Elsevier B.V.

ontents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 102. Review of water treatment efficacy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10

2.1. Chemical water treatments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 102.1.1. Chlorine . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 102.1.2. Chlorine dioxide . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 122.1.3. Ozone . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 132.1.4. Hydrogen peroxide and activated peroxygens . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 142.1.5. Copper . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 162.1.6. Silver. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 162.1.7. Bromine . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16

2.2. Physical water treatments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 162.2.1. Particle and membrane filters . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 162.2.2. Ultraviolet radiation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 182.2.3. Heat treatment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18

2.3. Ecological water treatments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21
2.3.1. Slow sand filtration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .2.3.2. Biosurfactants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .2.3.3. Constructed wetlands . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
∗ Corresponding author. Tel.: +1 352 273 4581; fax: +1 352 392 3870.E-mail addresses: [email protected] (R.E. Raudales), jennifer.parke@oregonsta

ttp://dx.doi.org/10.1016/j.agwat.2014.06.007378-3774/Published by Elsevier B.V.

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te.edu (J.L. Parke), [email protected] (C.L. Guy), [email protected] (P.R. Fisher).

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10 R.E. Raudales et al. / Agricultural Water Management 143 (2014) 9–28

3. Implications for research and effective water treatment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 234. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25

Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25 . . . . . .

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References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

. Introduction

The biological, physical, and chemical characteristics of a waterource impact its suitability for irrigation (Cook, 2000; FAO, 1994).rrigation water can be an inoculum source or dispersal mecha-ism for diverse biological problems including plant pathogensHong and Moorman, 2005; Ristaino and Gumpertz, 2000), algaeCamberato and Lopez, 2010; Dehghanisanij et al., 2005; Juanicot al., 1995) and biofilm-forming organisms (Adin and Sacks, 1991;an et al., 2009). Plant pathogens and other microbes are particu-

arly problematic when irrigating with surface or recirculated waterources (Gilbert et al., 1981; Runia, 1994a), and these water sourcesre increasingly being used in irrigation in order to conserve drink-ng water supplies (Obreza et al., 2010).

Diverse plant pathogens have been identified in irrigation waterncluding 17 species of Phytophthora, 26 species of Pythium, 27 gen-ra of true fungi, 8 species of bacteria, 10 viruses, and 13 speciesf plant parasitic nematodes (Hong and Moorman, 2005). Motileicroorganisms such as Pythium spp. and Phytophthora spp. may

e freely present in water, whereas plant pathogens that do notroduce swimming structures (for example, Rhizoctonia solani andhielaviopsis basicola) are more likely to be carried by bulk flow withoil debris in the water (Baker and Matkin, 1978).

Algae growth can also result from poor biological water qual-ty, and is a costly nuisance in agricultural systems (Camberatond Lopez, 2010; Schwarz and Krienitz, 2005). Algae can clogmitters, resulting in uneven irrigation distribution (Dehghanisanijt al., 2005; Juanico et al., 1995), reduce plant growth throughhe production of toxic substances (Schwarz and Krienitz, 2005;chwarz and Gross, 2004), and provide food and habitat for shoreies (Scatella stagnalis), which are vectors of plant pathogens (El-amalawi, 2007; Hyder et al., 2009). An impermeable-algae layeran form on the surface of the media reducing water permeabilityPeterson, 2001). Algae can create a worker hazard when cover-ng walk ways, and reduce aesthetic quality of ornamental pottedlants.

Biofilms are a complex matrix of polymers with pathogenicnd non-pathogenic microorganisms (Costerton et al., 1995; Maiert al., 2009). Organic compounds on the inside surface of pipesMaier et al., 2009) and soluble fertilizers provide nutrients for

icroorganisms and biofilm formation in irrigation pipes. Emittersre clogged directly when biofilm forms a physical barrier, or indi-ectly by the formation of precipitates with minerals such as iron,anganese and sulfur dissolved in water (Gilbert et al., 1981; Yan

t al., 2009). Biofilms are resistant to sanitizing treatment becausef their complexity and variability in structure and compositionBerry et al., 2006; Costerton et al., 1995; Tachikawa et al., 2009;iera et al., 1993).

A range of water treatments are available for management oficrobial water quality problems. Available treatments include

hemicals (chlorine, bromine, chlorine dioxide, ionized copper,opper salts, ionized silver, ozone, hydrogen peroxide, and perox-acetic acid), non-chemical or physical treatments (filtration, heat,nd ultraviolet (UV) radiation) and ecological alternatives (biosur-actants, constructed wetlands and slow sand filtration). Efficacy
f control of microbes depends on the target organisms, and theose with respect to concentration or intensity and contact timeEhret et al., 2001; Lane, 2004; Runia, 1995; Stewart-Wade, 2011;an Os, 2010). Water quality parameters, such as the concentration
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25

of suspended solids, presence of ions, pH, and temperature alsoaffect disinfestation strength of water treatments (Copes et al.,2004; Huang et al., 2011).

Literature reviews have been conducted on the presence ofplant pathogens in irrigation water (Hong and Moorman, 2005)and alternative water treatments to control microbial growth inirrigation (Ehret et al., 2001; Lane, 2004; Newman, 2004; Runia,1995; Stewart-Wade, 2011; Van Os, 2010). However, a comprehen-sive review of the alternatives to control plant pathogens, algae,and biofilms in irrigation systems is needed for irrigation spe-cialists designing water treatment options, in addition to plantpathologists and agronomists. The objective of this article was tosummarize the effective dose for controlling target waterbornemicroorganisms. This review includes a brief description of themode of action of each technology; the dose response for control ofpathogens, algae and biofilms; threshold concentrations leading tocrop phytotoxicity; and interactions with water contaminants andwater chemistry. Design considerations for effective water treat-ment, and research priorities were identified.

2. Review of water treatment efficacy

2.1. Chemical water treatments

2.1.1. Chlorine2.1.1.1. Mode of action. Chlorine is an oxidizer that removes elec-trons from reactants (such as a pathogen cell membrane), and inthe process chlorine becomes reduced to chloride (Cl−). Chlorinecan be applied to irrigation water as a gas (Cl2); as a liquid, mainlyas either sodium hypochlorite (NaOCl) or purified hypochlorousacid (HOCl); or as a solid, most commonly as calcium hypochlorite(Ca(ClO)2). The mode of action of chlorine for control of microor-ganisms is through both oxidation and chlorination (Deborde andvon Gunten, 2008). The two main pH-dependent forms of free chlo-rine in water are hypochlorous acid (HOCl, a strong oxidizer thatpredominates below pH 7.5), and hypochlorite (OCl−, a weak sani-tizer that predominates at higher pH) (Morris, 1966).

2.1.1.2. Dose response. Chlorine illustrates a wide range in dosage isrequired to control different pathogenic organisms, and life stageswithin organisms (Table 1). High mortality of oomycete zoosporeshas been observed with 2 mg L−1 of free chlorine (Hong et al.,2003; Lang et al., 2008). A dosage rate of 2 mg L−1 is typicallyused in irrigation (Fisher et al., 2008a,b). In contrast, mortalityof mycelia and sporangia of oomycetes required 4 mg L−1 with0.5 and 8 min contact time, respectively (Hong et al., 2003). Fusa-rium oxysporum and R. solani required 8 mg L−1 with 5 min contacttime and 10 mg L−1 with 10 min contact time to achieve mortalitygreater than 90%, respectively (Cayanan et al., 2009a). The concen-tration required to control bacterial pathogens ranged from 0.1to 4 mg L−1 (Poncet et al., 2001; Robbs et al., 1995; Roberts andMuchovej, 2009; Thompson, 1965). Between 5 and 30 mg L−1 con-trolled algae in studies by Chase and Conover (1993) and Rav-Achaet al. (1995). Commercial greenhouse recycled irrigation watertreated with 4 mg L−1 of chlorine (applied as sodium hypochlo-
rite) with 30 min contact time completely eliminated Cucumberleaf spot virus (CLSV) inoculum, but 3 mg L−1 had no effect on virusviability (Rosner et al., 2006). Nematodes are highly resistant tochlorination (Grech and Rijkenberg, 1991; Stanton and O’Donnell,

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11Table 1Efficacy of chlorine (hypochlorous acid) for control of waterborne microorganisms.

Chlorine form Organism (life stage) Treatment dose (mg L−1, contact time) Inactivated propagules(%)

Phytotoxicity Crop References

NaOCl Agrobacterium tumefaciens 4 mg L−1, 30 min 100% None observed Rosa sp. Poncet et al. (2001)NaOCl Algae (species not identified) 15–30 mg L−1 applied in subirrigation

solution once weekly for 9 weeksQualitative evaluationwith no algae observed

Not observed Ficus benjamina,Schefflera arboricolaand Dieffenbachiamaculata

Chase and Conover (1993)

NaOCl Botrytis cinerea 0.6 mg L−1, 10 min 100% N/A In vitro Machado et al. (2013)Cl2 Chlamydomonas sp. 5 mg L−1, 30 min 100% N/A In vitro Junli et al. (1997)NaOCl Chlorella vulgaris 2 mg L−1, 5 min 99% N/A In vitro Rav-Acha et al. (1995)NaOCl Cylindrocladium candelabrum 0.5 mg L−1, 10 min 100% N/A In vitro Machado et al. (2013)NaOCl Cucumber leaf spot virus (CLSV) 4 mg L−1, 30 min 100% Not measured Cucumis sativus Rosner et al. (2006)NaOCl Erwinia carotovora f. zeae 0.1 mg L−1, 1 min 100% Not observed Zea mays Thompson (1965)NaOCl Erwinia carotovora subsp. carotovora 0.4, 0.5, and 0.75 mg L−1 at pH 6, 7, and 8;

respectively, 2 min99% N/A In vitro Robbs et al. (1995)

NaOCl Fusarium foetens (conidia) 2.6 mg L−1, 15 min 100% N/A In vitro Elmer (2008)NaOCl Fusarium oxysporum 8 mg L−1, 1.5 min 90% N/A In vitro Cayanan et al. (2009a)NaOCl Geotrichum candidum (conidia) 20, 25, and >30 mg L−1 at pH 6, 7, and 8;

respectively, 2 min99% N/A In vitro Robbs et al. (1995)

NaOCl Meloidogyne javanica (eggs andjuveniles)

50,000 mg L−1, 60 min(eggs) or 2 mg L−1,24 h (juveniles)

75% (egg hatching),100% (juvenilemotility)

N/A In vitro Stanton and O’Donnell (1994)

Cl2 Microphorimidum sp. 5 mg L−1, 30 min 81% N/A In vitro Junli et al. (1997)NaOCl Phytophthora cactorum (zoospores) 0.3 mg L−1, 0.5 min 90% N/A In vitro Cayanan et al. (2009a)NaOCl Phytophthora capsici (zoospores) 2 mg L−1, 10 mina 100% N/A In vitro Roberts and Muchovej (2009)NaOCl Phytophthora citricola (zoospores) 1 mg L−1, 2 min 100% N/A In vitro Hong et al. (2003)NaOCl Phytophthora citrophthora (zoospores) 2 mg L−1, 2 min 100% N/A In vitro Hong et al. (2003)NaOCl Phytophthora cryptogea (zoospores) 2 mg L−1, 2 min 100% N/A In vitro Hong et al. (2003)NaOCl Phytophthora infestans (sporangia) 0.4 mg L−1, 1.5 min 95% N/A In vitro Cayanan et al. (2009a)NaOCl Phytophthora megasperma (zoospores) 2 mg L−1, 2 min 100% N/A In vitro Hong et al. (2003)NaOCl Phytophthora nicotianae (mycelia) 2 mg L−1, 8 min 98% N/A In vitro Hong et al. (2003)NaOCl Phytophthora nicotianae (sporangia) 4 mg L−1, 8 min 95% N/A In vitro Hong et al. (2003)NaOCl Phytophthora nicotianae (zoospores) 2 mg L−1, 2 min 100% N/A In vitro Hong et al. (2003)NaOCl Phytophthora sp. 5 mg L−1, 1 min 100% N/A In vitro Steddom and Pruett (2012)NaOCl Phytophthora sp. (chlamydospores and

zoospores)50 mg L−1 100% N/A In vitro Grech and Rijkenberg (1991)

Cl2 Phytophthora spp. b0.6 mg L−1 88% Not measured Container perennials Bush et al. (2003)NaOCl Phytophthora capsici (zoospores) 2 mg L−1, 2 min 100% N/A In vitro Hong et al. (2003)NaOCl Phytophthora capsici (zoospores) 2.42 mg L−1, 10 mina 100% N/A In vitro Granke and Hausbeck (2010)NaOCl Phytophthora cinnamomi (zoospores) 1 mg L−1, 2 min 100% N/A In vitro Hong et al. (2003)NaOCl Plasmodiophora brassicae 20 mg L−1, 10 min 47% Stunting and

intervenalchlorosis

Brassica oleracea Datnoff et al. (1987)

NaOCl Pythium aphanidermatum (zoospores) 0.5 mg L−1, 10 min 90% N/A In vitro Cayanan et al. (2009a)Not specified Pythium aphanidermatum (zoospores) 2 mg L−1, 2 min 99% N/A In vitro Hong and Richardson (2004)NaOCl Pythium aphanidermatum (zoospores) 0.5 mg L−1 at pH 6.3, 0.25 min, 764 mV ORP 90% N/A In vitro Lang et al. (2008)NaOCl Pythium dissotocum (zoospores) 0.5 mg L−1 at pH 6.3, 4 min, 766 mV ORP 90% N/A In vitro Lang et al. (2008)NaOCl Pythium spp. (zoospores) 2 mg L−1, 10 min 100% N/A In vitro Roberts and Muchovej (2009)Not specified Pythium sulcatum (zoospores) 2 mg L−1, 2 min 100% N/A In vitro Hong and Richardson (2004)NaOCl Ralstonia solanacearum 1.7 mg L−1, 10 min 100% N/A In vitro Machado et al. (2013)NaOCl Rhizoctonia solani (mycelia) 10 mg L−1, 10 min 90% N/A In vitro Cayanan et al. (2009a)Cl2 Ulothrix sp. 5 mg L−1, 30 min 100% N/A In vitro Junli et al. (1997)NaOCl Xanthomonas axonopoid 1.7 mg L−1, 10 min 100% N/A In vitro Machado et al. (2013)NaOCl Xanthomonas campestris pv. vesicatoria 2 mg L−1, 10 min 100% N/A In vitro Roberts and Muchovej (2009)

a Shorter contact times were not evaluated.b 0.6 mg L−1 was the average free chlorine of two year sampling period.

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994). Chlorine provides an example of the concentration and con-act time tradeoff for disinfestation chemicals, whereby a higheroncentration requires a shorter contact time for pathogen control,nd conversely the efficacy of a low chlorine dose is increased with

longer duration of exposure (Cayanan et al., 2009a; Hong et al.,003; Lang et al., 2008; Stanton and O’Donnell, 1994).

Although few published studies on the efficacy of chlorine torevent or destroy biofilms in irrigation can be found in the lit-rature, it appears that bacteria attached to biofilm surfaces areany times more resistant to chlorination than free bacteria (Bois

t al., 1997; LeChevallier et al., 1988). Treatment with 1 or 3 mg L−1

f chlorine resulted in 99.7% or 99.9% survival of bacteria withiniofilms, respectively (Bois et al., 1997).

.1.1.3. Phytotoxicity. Detrimental effects of chlorine on plantealth have been reported. Free chlorine at 2.4 mg L−1 appliedith overhead irrigation resulted in foliar phytotoxicity in several

ontainer-grown deciduous shrub species (Cayanan et al., 2009b).his dosage level is lower than the reported chlorine concentra-ions required to control some pathogens described in Table 1. Thisesult emphasizes the practical need to either increase contact timeith a lower chlorine concentration, for example in a holding tank

r baffle system, or remove active ingredient through technolo-ies such as activated carbon (Suidan et al., 1980) before reuse ofhlorinated water in order to avoid phytotoxicity risk.

.1.1.4. Sensitivity to water chemistry and contaminants. Chlorinefficacy decreases rapidly at high pH, or in the presence of organicnd nitrogen contaminants. The peak efficacy of chlorine againstathogens is observed around pH 6, because of the predominance ofypochlorous acid which is the strongest oxidizing form (Cherneyt al., 2006; Deborde and von Gunten, 2008; Lang et al., 2008). Oxi-ation reduction potential (ORP, or REDOX potential) measures thebility of oxidizing agents to remove electrons from microbial cellembranes and prompt microbial mortality (McPherson, 1993;

uslow, 2004; White, 1992). Plant pathogen mortality increasess pH decreases and ORP increases in a chlorinated solution (Langt al., 2008; Robbs et al., 1995). Combined inline measurement andontrol of pH, ORP, and active ingredient concentration providehe most efficient, reliable, and safe chlorination system. How-ver, many horticultural operators do not acidify their irrigationystem and do not regularly monitor water quality (Meador et al.,012).

Chlorine interacts with compounds containing ammonium orrganic nitrogen to form chloramines (Degrémont, 1979; Meadornd Fisher, 2013; Qiang and Adams, 2004; Weil and Morris, 1949).hloramines are sanitizing agents with a longer residual effect andreater stability at higher temperatures (>25 ◦C) than hypochlorouscid (Degrémont, 1979; Faust and Aly, 1983). However, chlo-amines require a longer contact time than hypochlorous acid toontrol waterborne pathogens (Degrémont, 1979). Phytotoxicityas been observed from chloramine application, with root necro-is occurring in hydroponic lettuce at 0.3 mg Cl L−1 combined with.4 mg NH4

+-N L−1 (Date et al., 2005).A 3:1 ratio of ammonium chloride to sodium hypochlorite was

ignificantly more effective in reducing bacteria attached to sur-aces than hypochlorous acid alone, presumably because of greaterenetration of the biofilm layers by the more stable chloraminesLeChevallier et al., 1988). Chloramines are likely to occur in pro-uction of containerized crops, given the common practice of

njecting both chlorine and ammonium-containing water-soluble
ertilizers. More research is needed to evaluate the efficacy of chlo-amines for control of microbes in irrigation systems, because mosturrent research has evaluated the treatment efficacy of hypochlor-us acid, rather than combined chlorine forms.
r Management 143 (2014) 9–28

Chlorine demand represents the decline in active ingredientlevel caused by contaminants such as organic matter, microorgan-isms, and ammonium in a water source from an applied activeingredient concentration to a lower residual level (Helbling andVanBriesen, 2007; Meador and Fisher, 2013). Peat at 50 mg L−1 insolution exerted a chlorine demand of 24% and 55% of the appliedconcentration after 2 and 60 min, respectively (Fisher et al., 2013).Biofilms in irrigation lines can greatly reduce the residual free chlo-rine measured at the most distant irrigation emitter comparedwith the applied dose (LeChevallier et al., 1988; Meador et al.,2012; Thompson, 1965). Oomycete zoospores were controlled with2 mg L−1 residual free chlorine (Hong et al., 2003). The level ofapplied chlorine required to achieve target residual concentrationsvaries depending on chlorine demand. Measurement of chlorine atboth the point of injection (to avoid overdosing and safety issues)and the furthest irrigation endpoint (to ensure adequate dosagefor microbial control) are therefore best management practicesfor chlorination. However, there are practical difficulties in thisapproach because combined chlorine compounds (including chlo-ramines) rapidly form within the irrigation distribution line andhave some sanitizing value, even though combined chlorine is notmeasured in free chlorine tests (Degrémont, 1979; Meador andFisher, 2013).

2.1.1.5. Regulatory. Chlorination of organic compounds can resultin toxic byproducts such as trihalomethanes and haloacetic acids,which US-EPA has identified as hazardous for human health(Deborde and von Gunten, 2008; Bull et al., 1990). Inhalation ofchlorine at 1 mg L−1 affects pulmonary function in human popula-tions with high sensitivity to chlorine (D’Alessandro et al., 1996),and delivery of chlorine in the gaseous form is highly regulated.The US-EPA established a maximum contaminant level goal (MCLG)for disinfectant and disinfectant byproducts, which represents themaximum level of contaminant in drinking water at which there isno known expected risk, is 4 mg Cl2 L−1 (US-EPA, 2013a).

2.1.2. Chlorine dioxide2.1.2.1. Mode of action. Chlorine dioxide has important technicaldifferences from hypochlorous acid, hypochlorite, and chlo-ramines. Chlorine dioxide, unlike chlorine gas, does not hydrolyzein water and remains as a dissolved gas (Amy et al., 2000; US-EPA,1999). The mode of action of chlorine dioxide is exclusively oxi-dation, and it does not chlorinate compounds like other chlorineforms (Amy et al., 2000). Chlorine dioxide has an oxidation poten-tial of 0.95 V for a 1 M solution at 25 ◦C, which is lower than chlorine(1.36 V) and ozone (2.07 V) (Degrémont, 1979), indicating a slowerreaction time.

2.1.2.2. Dose response. The effective dose to control microorgan-isms with chlorine dioxide (Table 2) ranged from 0.5 mg L−1 with2 min contact time for F. oxysporum conidia in municipal water(Mebalds et al., 1995) to an estimated dose of 57 mg L−1 for T. basi-cola conidia when the pH was 8.0 (Copes et al., 2004) (Table 2).Growers typically target about 0.25 mg L−1 residual concentrationat the emitter for continuous injection and 20–50 mg L−1 for shocktreatment to eliminate biofilms (Fisher et al., 2008c).

2.1.2.3. Phytotoxicity. A concentration of 2.5 mg L−1 chlorine diox-ide in pepper plants irrigated for 4 weeks is the lowest reportedlevel at which reduction of plant growth was observed (Rens, 2011).Ornamental bedding and woody plants receiving five foliar spraysin 3 day intervals at very high doses (≥50 mg L−1) of chlorine diox-
ide did not show phytotoxicity (Copes et al., 2003). Symptomsassociated with phytotoxicity caused by chlorine dioxide includedyellowing of the leaf margin or tip (early symptoms), necrotic leaftips and margins, necrotic spots and blotches on leaves and flowers,

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Table 2Efficacy of chlorine dioxide for control of waterborne microorganisms.

Organism (life stage) Treatment dose (mg L−1, contact time) Inactivatedpropagules (%)


Alternaria zinniae (cfu) 2 mg L−1, 12 min 90% N/A In vitro Beardsell and Bankier (1996)Ankistrodesmus sp. 5 mg L−1, 30 min 100% N/A In vitro Junli et al. (1997)Chlamydomonas sp. 5 mg L−1, 30 min 75% N/A In vitro Junli et al. (1997)Chlorella vulgaris (green algae) 2 mg L−1, 5 min 99% N/A In vitro Rav-Acha et al. (1995)Colletotrichum capsici (spores) 0.5 mg L−1, 2 min (municipal water)a 100% N/A In vitro Mebalds et al. (1995)

4 mg L−1, 2 min (surface water)Erwinia carotovora subsp. carotovora 1.3 mg L−1, 10 min 90% N/A In vitro Yao et al. (2010)Fusarium oxysporum f.sp. narcissi

(macro and micro- conidia)2.2 mg L−1, 0.5 min (pH 8.0)b 90% N/A In vitro Copes et al. (2004)

0.8 mg L−1, 0.5 min (hard water with100 mg L−1 N)

Fusarium oxysporum (conidia) 0.5 mg L−1, 2 min (municipal water)c 99% N/A In vitro Mebalds et al. (1995)2 mg L−1, 2 min (surface water)

Microphorimidum sp. 5 mg L−1, 30 min 100% N/A In vitro Junli et al. (1997)Phorimidium sp. 5 mg L−1, 30 min 100% N/A In vitro Junli et al. (1997)Phytophthora capsici (zoospores) 3 mg L−1, 1 min 7– 24% N/A In vitro Lewis Ivey and Miller (2013)Phytophthora cinnamomi

(chlamydospores)9 mg L−1, 4 min 92% N/A In vitro Beardsell and Bankier (1996)

Phytophthora cinnamomi (zoospores) 0.9 mg L−1,12 min 100% N/A In vitro James et al. (1996)Phytophthora cinnamomi (zoospores) 1 mg L−1, 2 min (municipal water)d 100% N/A In vitro Mebalds et al. (1995)

4 mg L−1, 2 min (surface water)Pythium ultimum (oospores) 0.5 mg L−1, 2 min 99% N/A In vitro Beardsell et al. (1996)Ralstonia solanacearum 1.3 mg L−1, 10 min 99% N/A In vitro Yao et al. (2010)Thielaviopsis basicola (aleuriospores) 47 mg L−1, 0.5 min (pH 5.0)b N/A In vitro Copes et al. (2004)

57 mg L−1, 0.5 min (pH 8.0)b

Thielaviopsis basicola (conidia) 2.1 mg L−1, 0.5 min (pH 5.0)b 90% N/A In vitro Copes et al. (2004)2.0 mg L−1, 0.5 min (pH 8.0)b

Ulothrix sp. 5 mg L−1, 30 min 100% N/A In vitro Junli et al. (1997)Xanthomonas campestris pv. campestris 3 mg L−1 daily overhead irrigatione 90% Not measured Cauliflower

seedlingsKrauthausen et al. (2011)

a Residual concentration of 0.4 mg L−1 (municipal water), 1.8 mg L−1 (surface water).b Estimated LD90 values.

).).

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c Residual concentration of 0.4 mg L−1 (municipal water), 1 mg L−1 (surface waterd Residual concentration of 0.9 mg L−1 (municipal water), 2 mg L−1 (surface watere Residual concentration of 0.21 mg L−1.

lant death, and overall reduction of plant growth (Carrillo et al.,996; Copes et al., 2003; Rens, 2011).

.1.2.4. Sensitivity to water chemistry and contaminants. Organicatter and inorganic ions in solution, for example, with sur-

ace water sources, exert a demand on chlorine dioxide (Mebaldst al., 1995). The presence of 50 mg L−1 of peat in the solutionncreased the demand of chlorine dioxide up to 36.3% and 52.5%fter 2 and 60 min, respectively (Fisher et al., 2013). Chlorineioxide is less sensitive than chlorine to solution pH (Benardet al., 1965; Yao et al., 2010), although a chlorine dioxide solu-ion required higher concentrations to achieve the same level oflant pathogen control at pH 8 than pH 5 (Copes et al., 2004).he presence of micronutrients in the solution also increasedhe required chlorine dioxide concentration to achieve pathogen

ortality (Copes et al., 2004). The combination of micronutrientsith water hardness (magnesium, calcium, and bicarbonate) anditrogen increased the concentration of chlorine dioxide requiredo kill fungal pathogens in water at pH 5 and decreased theoncentration required to kill pathogens at pH 8 (Copes et al.,004). As a dissolved gas, the maximum concentration of dissolvedhlorine dioxide decreases with increasing temperature (US-EPA,009).

.1.2.5. Regulatory. Unlike chlorine, the reaction of chlorine diox-de with organic matter does not result in trihalomethanes (US-EPA,999). However, direct ingestion or inhalation of chlorine dioxide
r its byproducts (chlorites and chlorates) can result in irritationf the digestive tract or chronic respiratory deficiencies, and skinnd nasal irritations (US-EPA, 2000). The maximum contaminantevel goal for drinking water for chlorites and chlorates together
should not exceed 1 mg L−1 (Bull et al., 1990; US-EPA, 1999). Themaximum residual disinfectant level (MRDL) for chlorine dioxideis 0.8 mg L−1 in drinking water (US-EPA, 2013a).

2.1.3. Ozone2.1.3.1. Mode of action. Ozone (O3) acts by direct oxidation orthrough the production of short-lived hydroxyl free radicals andsuperoxide ions (Hoigné and Bader, 1976; US-EPA, 1999). Ozonehas an oxidation reduction potential of 2.07 V, which is the high-est of water treatment oxidizers (Degrémont, 1979). Ozone isan unstable gas which must be generated onsite, usually viacorona discharge or ultraviolet radiation (Degrémont, 1979; US-EPA, 1999). Briefly, the corona discharge method passes highvoltage through two separated electrodes causing the release ofelectrons to the gap between electrodes. The energy from the elec-trons dissociates the oxygen from the environment resulting inozone formation from the combination of oxygen atoms (O−) withoxygen molecules (O2) (US-EPA, 1999). In contrast, UV radiationozone generators use UV light to split the oxygen molecule andform ozone. A residual dose under 1 mg L−1 is typically suggestedfor greenhouse irrigation (Hayes et al., 2009).

2.1.3.2. Dose response. Plant pathogens varied widely in resistanceto oxidation by ozone, with the required ozone dose ranging from0.5 mg L−1 with 1 min contact time for Pectobacterium carotovo-rum subsp. carotovorum (Kobayashi et al., 2011) to 100 mg L−1 with30 min contact time for Tomato mosaic virus (ToMV) (Runia, 1994a)
(Table 3). The minimum reported doses to control bacteria, fungi,oomycetes and virus were 0.5, 0.7, 0.8 and 7.9 mg L−1 ozone withcontact time of 1, 16, 8, and 75 min, respectively (Beardsell andBankier, 1996; Kobayashi et al., 2011; Runia, 1994a).


Table 3Efficacy of ozone for control of waterborne plant pathogens.

Organism (life stage) Treatment dose (mg L−1, contact time) Inactivatedpropagules (%)


Acidovorax avenae subsp. citrulli 0.05 mg L−1 a Not measured Citrullus lanatus Hopkins et al. (2009)Alternaria zinniae (spores) 0.7 mg L−1, 16 minb 90% N/A In vitro Beardsell and Bankier (1996)Corynebacterium michiganense 1.1 mg L−1 for 55 minc N/A In vitro Vanachter et al. (1988)Cucumber green mottle mosaic

virus (CGMMV)7.9 mg L−1 for 75 min (ORP 673 mV) 100%d Not measured Cucumis sativus Runia (1994a)

Fusarium oxysporum (conidia) 1 mg L−1, 10 min 99% N/A In vitro Igura et al. (2004)Fusarium oxysporum (conidia) 1.8 mg L−1, 4 minb 99% N/A In vitro Beardsell and Bankier (1996)Fusarium oxysporum f. sp.

melonis1 mg L−1, ≥0.5 min 100% N/A In vitro Kobayashi et al. (2011)

Pectobacterium carotovorumsubsp. carotovorum

0.5 mg L−1, 1 min 100% N/A In vitro Kobayashi et al. (2011)

Phytophthora cinnamomi(chlamydospores)

0.8 mg L−1, 8 minb 99% N/A In vitro Beardsell and Bankier (1996)

Pythium ultimum (oospores) 1.2 mg L−1 for 2 minb 95% N/A In vitro Beardsell and Bankier (1996)Tomato mosaic virus (ToMV) 100 mg L−1 for 30 min (ORP 517 mV) 99%d Not measured Nicotiana

glutionosaRunia (1994a)

a Did not decrease fruit blotch symptoms.

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b Residual concentration in municipal water.c Residual concentration in nutrient solution containing Fe-DTPA.d Reduction in virus infectivity.

.1.3.3. Phytotoxicity. Woody ornamentals irrigated overhead withater containing ≥0.9 mg L−1 ozone at the emitter on a daily

asis for 6 weeks showed phytotoxicity symptoms, but no neg-tive effects were observed at 0.5 mg L−1 (Graham et al., 2009).ymptoms associated with ozone phytotoxicity were leaf injury,eduction of leaf area, shoot weight (fresh and dry), shoot height,nd root dry weight.

.1.3.4. Sensitivity to water chemistry and contaminants. Man-anese, iron, and micronutrient chelates can be oxidized by ozone,reating a demand for active ingredient (Ohashi-Kaneko et al.,009; Vanachter et al., 1988). Demand for ozone active ingredientrom the nutrient solution decreased control of F. oxysporum andorynebacterium michiganense by ozone (Vanachter et al., 1988).zone efficacy was lower at pH 8.0 than pH 7.2 in laboratory exper-

ments (Domingue et al., 1988). Like other dissolved gases, theaximum concentration of dissolved ozone in solution decreases

s temperature increased from 15 ◦C to 30 ◦C (Kobayashi et al.,011).

.1.3.5. Regulatory. Ozone is a regulated atmospheric pollutant foruman health risk (US-EPA, 1999), and systems must be designedo avoid off-gassing of concentrated ozone into the work environ-

ent. Because of its reactive nature, ozone up to 15 mg L−1 wasapidly depleted to undetectable levels, after a single pass through

rockwool slab (Graham et al., 2011, 2011b). Although ozone nor-ally breaks down into oxygen, in some situations carcinogenic

y-products such as bromate may result from ozonation (US-EPA,999).

.1.4. Hydrogen peroxide and activated peroxygens

.1.4.1. Mode of action. Hydrogen peroxide (H2O2) can be usedirectly as an oxidizing water treatment. Hydrogen peroxide is alson active ingredient in the class of “activated peroxygen” prod-cts where H2O2 is combined with organic acids such as aceticcid to form more stable and effective sanitizing molecules includ-ng peroxyacetic acid (Hopkins et al., 2009; Nedderhoff, 2000;ewman, 2004; Pettitt, 2003; Van Os, 2010). Hydrogen peroxideas an oxidation potential of 1.76 V (Degrémont, 1979), how-
ver the relationship between hydrogen peroxide concentrationnd ORP is complex (Suslow, 2004). Therefore hydrogen peroxideosage is normally tested using colorimetric methods rather thanRP (Suslow, 2004).
2.1.4.2. Dose response. The effective dose to control microor-ganisms with hydrogen peroxide-based products ranged from12.3 mg L−1 hydrogen peroxide combined with 8 mg L−1 perox-yacetic acid for control of algae (contact time not specified)(Choppakatla, 2009) to 185 mg L−1 hydrogen peroxide plus120 mg L−1 peroxyacetic acid with 1 minute contact time to controlPhytophthora sp. (Steddom and Pruett, 2012) (Table 4). The requireddose for water treatment varies between commercial activated per-oxygen products, because the commercial products vary in the ratioof hydrogen peroxide to peroxyacetic and other acids.

2.1.4.3. Phytotoxicity. Phytotoxicity thresholds for hydrogen per-oxide have been observed between 8 mg L−1 applied in thenutrient solution of soilless lettuce seedlings (Nedderhoff, 2000) to125 mg L−1 applied in the nutrient solution in cucumber plants onrockwool (Vänninen and Koskula, 1998). Phytotoxicity thresholdsfor other activated peroxygens remain to be established. Symp-toms associated with hydrogen peroxide toxicity included leafscorching (Vänninen and Koskula, 1998), reduced plant growth(Nedderhoff, 2000) and plant mortality (Van Wyk et al., 2012).Symptoms associated with very high concentrations of acti-vated peroxygens included necrosis and dehydration of leaf andflowers, and spots and blotches on the leaves (Copes et al.,2003).

2.1.4.4. Sensitivity to water chemistry and contaminants. Hydrogenperoxide concentration is lowered by increased temperature andlight levels, alkaline pH and some metal ions (Degrémont, 1979).Exposure of an activated peroxygen solution to 50 mg L−1 of peatin the solution did not reduce active ingredient concentrationafter 2 or 60 min (Fisher et al., 2013). However, higher concentra-tions (10 g L−1) of peat reduced the amount of hydrogen peroxideand peroxyacetic acid from activated peroxygens by 33% and 50%,respectively, after 4 h contact time (Huang et al., 2011).

2.1.4.5. Regulatory. The reaction of hydrogen peroxide withorganic matter in solution results in end products of water andoxygen. Therefore, hydrogen peroxide is considered a safe alterna-
tive for workers and the environment compared with some otherwater treatment alternatives (Nedderhoff, 2000), although a shortre-entry interval is required in greenhouses following applicationof commercial activated peroxygen products.

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15

Table 4Efficacy of activated peroxygens, hydrogen peroxide and peracetic acid for control of waterborne plant pathogens.

Active Ingredient Organism (life stage) Treatment dose (mg L−1, contact time) Inactivated propagules (%) Phytotoxicity Crop References

Peroxyacetic acid Acidovorax avenaesubsp. citrulli

80 mg L−1a 50% e Not observed Citrullus lanatus Hopkins et al. (2009)

Hydrogen peroxide Algae 125 mg L−1a N/A b Scorching of leaf margins,wilting, reduced number ofleaves and dry weight

Cucumis sativus Vänninen and Koskula (1998)

Hydrogen peroxide andperoxyacetic acid

Algae (Microcystis sp.,Scenedesmus sp., andChlorococcum sp.)

12.3 mg L−1 hydrogenperoxide + 8 mg L−1 peroxyacetic acida

100% N/A In vitro Choppakatla (2009)

Hydrogen peroxide Fusarium circinatum 400 mV (ORP) for 6 h (specific H2O2

dose was not specified)100% Not observed. High mortality

(>89%) was observed withhigher doses (>450 mV)

Pinus spp. Van Wyk et al. (2012)


Fusarium foetens(conidia)

135 mg L−1 hydrogenperoxide + 10 mg L−1 of peroxyaceticacid, 15 min

100% N/A In vitro Elmer (2008)


Fusarium foetens(conidia)

37 mg L−1 hydrogenperoxide + 24 mg L−1 of peroxyaceticacid, 15 min

100% N/A In vitro Elmer (2008)


Fusarium oxysporum f.sp. lycopersici (conidia)

100 mg L−1, 5 min 100% d d Runia (1995)


Phytophthora sp. 185 mg L−1 hydrogenperoxide + 120 mg L−1 peroxyaceticacid, 1 min

100% mortality in nurseryrunoff and pond water

N/A In vitro Steddom and Pruett (2012)

88% in greenhouse runoffHydrogen peroxide and

peroxyacetic acidPhytophthora sp. 12.3 mg L−1 hydrogen

peroxide + 8 mg L−1 peroxyacetic acida100% N/A In vitro Choppakatla (2009)


Pythium spp. 12.3 mg L−1 hydrogenperoxide + 8 mg L−1 peroxyacetic acida

100% N/A In vitro Choppakatla (2009)


ToMV 400 mg L−1 (specific concentrations ofH2O2 or PAA not specified)c

99% d d Runia (1995)

a Contact time not specified.b Algae control estimated based on a scale index.c Applied daily as overhead irrigation.d Not specified.e Reduction in bacterial fruit blotch.

1 Wate

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.1.5. Copper

.1.5.1. Mode of action. Copper is an essential element for plantrowth and other eukaryotes and prokaryotes (Evans et al., 2007;arschner, 1995). However, high concentrations of copper can

ind to protein prosthetic groups and disrupt normal cellular pro-ein structure, negatively affecting microbial and plant metabolismDegrémont, 1979; Evans et al., 2007; Flemming and Trevors, 1989;hurman et al., 2009). Copper can be delivered for water treatmentn the form of copper ions via electrolysis (ionized copper) or disso-ution of copper salts. Copper salts have been used as fungicide asarly as the 1880s (Agrios, 2005) and as an algaecide since the early900s (Flemming and Trevors, 1989; Thurman et al., 2009). Com-ercial copper algaecides include a number of inorganic or organic

opper molecules. In electrolysis, positively charged copper ions areisplaced at the anodes (Stewart-Wade, 2011).

.1.5.2. Dose response. The effective dose to control microorgan-sms by copper supplied via electrolysis ranged between 2 and

mg L−1 for several microorganisms (Table 5). In many cases, anxtended contact time of several hours was required for control.opper algaecide salts varied widely in the required dose for con-rol of Phytophthora capsici zoospores (Granke and Hausbeck, 2010)r Erwinia carotovora subsp. carotovora (Gracia-Garza et al., 2002).reenhouses and nursery growers typically apply 1 mg Cu L−1

rom ionized copper to prevent algae buildup and control plantathogens (Zheng et al., 2005).

.1.5.3. Phytotoxicity. Reported phytotoxicity thresholds causedy copper applications in water ranged between 0.08 mg L−1 in taroColocasia esculenta) applied in the nutrient solution of a hydro-onic system (Hill et al., 2000) to 5.0 mg L−1 in woody ornamentalspplied in the nutrient solution of plants grown in sand (Kuhnsnd Sydnor, 1976). Calla lilies (Zantedeschia spp.) overhead irrigatedith water containing commercial copper bactericides or reagent

rade copper chloride resulted in shorter plants with fewer flow-rs compared with plants that were sub-irrigated with the sameolution (Gracia-Garza et al., 2002).

.1.5.4. Sensitivity to water chemistry and contaminants. Peat at0 mg L−1 reduced the applied 2 mg L−1 free copper from eitheropper salts or ionized copper by only 3.4% and 5.5%, respectively,fter 1 h contact time (Fisher et al., 2013). Ionized copper was lessffective at controlling Phytophthora root rot in gerberas when theutrient solution contained iron chelates (Fe-HEEDTA) comparedith iron salts (FeSO4) (Toppe and Thinggaard, 1998), presumably

ecause of substitution reactions of copper with the iron chelate.onized copper and copper salts were less effective at controllinglgae when the nutrient solution contained Fe-EDDHA instead ofe-EDTA (Mohammad-Pour et al., 2011).

.1.5.5. Regulation. Copper formulations are regulated by US-EPAs pesticides (US-EPA, 1999). Based on the Safe Drinking Waterct, the maximum contaminant level goals for copper in water is.3 mg L−1 (US-EPA, 2013a).

.1.6. Silver

.1.6.1. Mode of action. Silver ions can be generated in the sameay as copper either through electrolysis (Stewart-Wade, 2011)

r as a dissolved salt. Silver ions disrupt membranes of microor-anisms, resulting in cell lysis (Slade and Pegg, 1993; Miller andcCallan, 1957).

.1.6.2. Dose response. The efficacy to control plant pathogens withilver nitrate ranged from 0.07 mg L−1 for conidia of F. oxysporum f.p. lycopersici to 0.5 mg L−1 for conidia of F. oxysporum f. sp. dianthi

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(Slade and Pegg, 1993) (Table 6). Combined silver and copper ion-ization by electrolysis has been widely used as a water disinfectionmethod in hospitals for control of Legionnaires’ disease (Lin et al.,2011; Perez Cachafeiro et al., 2007; Rohr et al., 1999; Stout, 2003).Ionized silver was reported to be ineffective to control Alternaria,Fusarium spp. and Tobacco mosaic virus (TMV) (Stewart-Wade,2011).

2.1.6.3. Phytotoxicity. Little has been documented about using sil-ver alone or in combination with copper as a water treatmentin plant production (Stewart-Wade, 2011). However, silver appli-cation has several potential impacts on plant health includinginhibiting ethylene responses (Bradford and Dilley, 1978), reducingthe number of staminate flowers (Hallidri, 2004), reducing petalabscission (Cameron and Reid, 1983), and reducing plant height(Karakaya and Padem, 2012).

2.1.6.4. Regulation. Silver ions from salts and electrolysis are reg-ulated by US-EPA as pesticides (US-EPA, 1999). Silver is listed as asecondary contaminant, which means that it is not a threat to healthand therefore monitoring is voluntary. The suggested maximumlevel goal for drinking water is of 1 mg L−1 (US-EPA, 2013a).

2.1.7. Bromine2.1.7.1. Mode of action. Bromine is an oxidizer with oxidationpotential of 1.33 V or 0.70 V in the form of hypobromous acid (HBrO)or bromide (BrO−), respectively (Degrémont, 1979).

2.1.7.2. Dose response. Chase (1990, 1991) evaluated applicationof bromine in overhead irrigation with a range of both ornamen-tal plant species and pathogens, with variable levels of pathogencontrol at 25–60 mg L−1 (Table 7). Weekly applications of bromineapplied at 15 mg L−1 in sub-irrigation for the first 5 weeks and then30 mg L−1 for 9 weeks did not prevent algae buildup (Chase andConover, 1993). Bromine applied at 0.27 g L−1 was not effective inremoving T. basicola from plastic, wood and metal surfaces (Copesand Hendrix, 1996).

2.1.7.3. Phytotoxicity. Several plant species (Aeschynanthus pul-cher, Dracaena marginata, Ficus benjamina, Hedera helix, Hibiscusrosa-sinensis, Saintpaulia ionantha, and Schlumbergera truncate) irri-gated overhead with doses between 50 and 60 mg L−1 presentedsymptoms that included distortion of immature leaves and abscis-sion, severe necrosis, chlorosis on mature and immature leaves,stunting, and white spots on flowers (Chase, 1991). A lower con-centration (15 mg L−1) applied through sub-irrigation for 5 weeksdid not reduce plant quality of F. benjamina, Schefflera arboricolaand Dieffenbachia maculata (Chase and Conover, 1993).

2.1.7.4. Regulation. The reaction of bromine with organic matterresults in the formation of halogenated organics which are con-sidered detrimental for human health (US-EPA, 1999). Registeredbromine products do not generate bromate ion (BrO3

−), which isconsidered a possible carcinogenic agent and has a maximum con-centration in drinking water of 0.010 mg L−1 (US-EPA, 1999).

2.2. Physical water treatments

2.2.1. Particle and membrane filters2.2.1.1. Mode of action. The mechanisms of particle removal withfiltration consist of straining, impaction, interception, adhesion,and flocculation (Levine et al., 1985). Filters suitable for removal
of microorganisms from water are either membrane filters withsmall pore size (<10 �m), or slow sand filters (which are describedunder the Section 2.3 of this article) (Ehret et al., 2001; Stewart-Wade, 2011; Ufer et al., 2008; Van Os, 2010). Membrane filters can

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17Table 5Efficacy of copper for control of waterborne plant pathogens.

Copper source Organism (life stage) Treatment dose (mg L−1,contact time)

Inactivated propagules (%) Phytotoxicity Crop References

Ionized copper Acidovorax avenae subsp. citrulli 1.5 mg L−1, applied dailya 97%a Not measured Citrullus lanatus Hopkins et al. (2009)Ionized copper Agrobacterium tumefaciens 2 mg L−1, 24 h or 99% N/A b Wohanka et al. (2006)

4 mg L−1, 4 hIonized copper Agrobacterium tumefaciens 4 mg L−1, 1 h 53% N/A b Wohanka et al. (2006)Ionized copper Algae (unidentified species) 2 mg L−1 99% N/A In vitro Mohammad-Pour et al. (2011)Ionized copper Clavibacter michiganensis 2 mg L−1, 2 h 91% N/A b Wohanka and Fehres (2007a)Ionized copper Clavibacter michiganensis 2 and 4 mg L−1, 1 h 54% N/A b Wohanka and Fehres (2007a)Ionized copper Erwinia carotovora subsp. carotovora 2 mg L−1, 1 h 96% N/A b Wohanka et al. (2007)Ionized copper Erwinia carotovora subsp. carotovora 2 mg L−1 and 4 mg L−1, ≤5 min 0% N/A b Wohanka et al. (2007)Ionized copper Fusarium oxysporum f.sp. cyclaminis (conidia) 1–3 mg L−1, 1–24 h 0% N/A b Wohanka and Fehres (2006a)Ionized copper Phytophthora cinnamomi (zoospores) 0.28 mg L−1 84% Not measured Hedera helix Toppe and Thinggaard (2000)Ionized copper Phytophthora cryptogea (zoospores) 0.28 mg L−1 69%a Not measured Gerbera jamesonii Toppe and Thinggaard (1998)Ionized copper Pythium aphanidermatum (zoospores) 4 mg L−1, 1 h 0% N/A b Wohanka and Fehres (2006b)Ionized copper Ralstonia solanacearum Race 3 2 mg L−1, 1 h 96% N/A b Wohanka and Fehres (2007b)Ionized copper Ralstonia solanacearum Race 3 2 and 4 mg L−1, ≤5 min <1% N/A b Wohanka and Fehres (2007b)Ionized copper Trichoderma asperellum (conidia) 4 mg L−1, 24 h 0% N/A b Wohanka et al. (2009)Ionized copper Xanthomonas hortorum pv. pelargonii 2 mg L−1, 4 h 97% N/A b Wohanka and Fehres (2006c)Ionized copper Xanthomonas hortorum pv. pelargonii 0.5 and 1 mg L−1, 24 h 41% N/A b Wohanka and Fehres (2006c)Copper hydroxide Acidovorax avenae subsp. citrulli 0.43 mg L−1; applied weekly 50%a Not measured Citrullus lanatus Hopkins et al. (2009)Copper nitrate Algae 4 mg L−1 99% N/A In vitro Mohammad-Pour et al. (2011)Copper sulfate Algae 2 mg L−1, weekly c Good and marketable

plant quality dDieffenbachia maculata,Ficus benjamina L.,Schefflera arboricola

Chase and Conover (1993)

Copper chloride Erwinia carotovora subsp. carotovora 32 mg L−1a 1%a Reduction in height, freshmass and root growth e

Zantedeschia spp. Gracia-Garza et al. (2002)

Copper chloride Erwinia carotovora subsp. carotovora 4 mg L−1, 30 min 99% N/A In vitro Gracia-Garza et al. (2002)Copper hydroxide Erwinia carotovora subsp. carotovora 5.2 mg L−1 13% Reduction in height, fresh

mass and root growth eZantedeschia spp. Gracia-Garza et al. (2002)

Copper hydroxide Erwinia carotovora subsp. carotovora 1 mg L−1, 30 min 100% N/A In vitro Gracia-Garza et al. (2002)Copper oxychloride Erwinia carotovora subsp. carotovora 8 mg L−1 15% Reduction in height, fresh


Copper oxychloride Erwinia carotovora subsp. carotovora 2 mg L−1, 30 min 100% N/A In vitro Gracia-Garza et al. (2002)Copper sulfate Erwinia carotovora subsp. carotovora 4 mg L−1a 3% Reduction in height, fresh


Copper sulfate Erwinia carotovora subsp. carotovora 0.5 mg L−1, 30 min 100% N/A In vitro Gracia-Garza et al. (2002)Copper carbonate Phytophthora capsici (zoospores) 1.6 mg L−1, 2 h 100% N/A In vitro Granke and Hausbeck (2010)Copper citrate and copper

gluconatePhytophthora capsici (zoospores) 1.7 mg L−1, 2 h 40% N/A In vitro Granke and Hausbeck (2010)

Copper ethanolamine Phytophthora capsici (zoospores) 1.6 mg L−1, 2 h 100% N/A In vitro Granke and Hausbeck (2010)Copper sulfate pentahydrate Phytophthora capsici (zoospores) 1.6 mg L−1, 2 h 100% N/A In vitro Granke and Hausbeck (2010)Copper sulfate pentahydrate Phytophthora capsici (zoospores) 0.5 mg L−1, 2 h >90% N/A In vitro Granke and Hausbeck (2010)Copper triethanolamine and

copper hydroxidePhytophthora capsici (zoospores) 1.7 mg L−1, 2 h 100% N/A In vitro Granke and Hausbeck (2010)

Copper carbonate Phytophthora citricola, P. citrophora, P.cryptogea, P. nicotianae, P. palmivora, P.ramorum (chlamydospores, sporangia andzoospores)

0.8 mg L−1, 30 min 100% N/A In vitro Colburn and Jeffers (2010)

Coppertriethanolamine + copperhydroxide

Phytophthora citricola, P. citrophora, P.cryptogea, P. nicotianae, P. palmivora, P.ramorum (chlamydospores, sporangia andzoospores)

1 mg L−1, 30 min 100% N/A In vitro Colburn and Jeffers (2010)

a Applied with irrigation, reduction in disease incidence.b Experiments carried out in greenhouse conditions not including crops.c Qualitative assessment rating 2: slight green growth (1: None, white bench; 5: complete green surface).d Average qualitative rating 4.2 for all crops (1: dead, 5: excellent quality).e General results for copper phytotoxicity. Results varied between overhead and subirrigation and by copper source.


Table 6Efficacy of silver for control of water borne plant pathogens.

Organism (life stage) Treatment dose(mg L−1, contact time)

Inactivatedpropagules (%)


Fusarium oxysporum f. sp. dianthi (conidia) 0.5 mg L−1, 18 h 100% N/A In vitro Slade and Pegg (1993)Fusarium oxysporum f. sp. lycopersici (conidia) 0.07 mg L−1, 18 h 100% N/A In vitro Slade and Pegg (1993)Phytophthora cryptogea (zoospores) 0.08 mg L−1, 18 h 100% N/A In vitro Slade and Pegg (1993)Phytophthora nicotianae (zoospores) 0.1 mg L−1, 18 h 100% N/A In vitro Slade and Pegg (1993)Pythium aphanidermatum (zoospores) 0.08 mg L−1, 18 h 100% N/A In vitro Slade and Pegg (1993)Thielaviopsis basicola 0.1 mg L−1, 18 h 100% N/A In vitro Slade and Pegg (1993)

10

b(dtrps

osPu(wdt1aaep(

2r1PHafiocHV

2fimb2bdtbiitsla

2t

Verticillium albo-atrum 0.1 mg L−1, 18 h

e classified as micro- (0.1–10 �m), ultra- (0.1–0.002 �m), nano-0.0005–0.002 �m) filtration, or reverse osmosis (<0.0005 �m)epending on pore size (Van der Bruggen et al., 2003). Particle fil-ers with larger pore sizes and rapid sand filters are important toeduce clogging of membrane filters by particles, to remove soil andlant material that may contain pathogens, and to reduce chemicalanitizing demand of the irrigation water.

Microbial propagules differ in size depending on the type ofrganism and the life stage, which should be considered whenelecting between filtration systems. For example, the length ofhytophthora sporangia ranges from 10 �m (Phytophthora katsurae)p to 171 �m (Phytophthora erythroseptica var. erythroseptica)Erwin and Ribeiro, 1996). Zoospores of Phytophthora and Pythium,hich emerge from sporangia, are approximately 7–10 �m iniameter (Drechsler, 1952; Hardham, 2001). Mycelia of Phytoph-hora spp. have a diameter between 5 and 8 �m (Erwin and Ribeiro,996). Fusarium sp. macroconidia are approximately 50 �m longnd 7 �m wide and approximately 20 �m in diameter (Toussounnd Nelson, 1976). Bacteria range between 0.6 and 3.5 �m in diam-ter (Agrios, 2005). Viruses vary in size from 0.03 �m (sphericallant virus), 0.3 by 0.018 �m (rigid rod shape), and up to 2 �m longfilamentous virus) (Gergerich and Dolja, 2006).

.2.1.2. Efficiency of removal. Membrane filters were effective atemoving bacteria and fungi (Table 8), and also ToMV (Runia,995). Filters with larger, 5–7 �m, pores were effective at removingythium aphanidermatum zoospores (Goldberg et al., 1992; Tu andardwood, 2005) (Table 8). Membrane filtration was most effectivet controlling pathogens when combined in a series of multi-stagelters from larger to smaller pore size, and in combination withther water treatments that have other modes of action, such ashlorine (Goldberg et al., 1992; Machado et al., 2013; Moens andendrickx, 1992; Ohtani et al., 2000; Schuerger and Hammer, 2009;an der Bruggen et al., 2003).

.2.1.3. Sensitivity to water chemistry and contaminants. Membranelters can be clogged by suspended solids (sand, silt, organicatter), chemical precipitates (Fe, Mn, carbonates, pesticides), or

acteria and algae (Moens and Hendrickx, 1992; Yiaosumi et al.,005). Pre-filtration of suspended solids is therefore essentialefore membrane filtration to prevent membrane clogging (Vaner Bruggen et al., 2003). Reverse osmosis removes nutrients fromhe solution, which is a disadvantage if the nutrient solution wille recirculated (Runia, 1995), but salt removal is an advantage

n irrigation water containing excess sodium or chloride. Theres increasing resistance to water flow, and increased need for fil-er cleaning, as filter pore size decreases. Efficacy at a given poreize also decreases as flow rate increases. Together these factorsimit use of membrane filters for high irrigation volume and flow
pplications.
.2.1.4. Regulation. There is no federal regulation on membrane fil-ers as a water treatment technology, but disposal of liquid and

0% N/A In vitro Slade and Pegg (1993)

solids wastes (including brine and used membrane filters) frommembrane filtration are regulated at the state level in the UnitedStates (US-EPA, 2005).

2.2.2. Ultraviolet radiation2.2.2.1. Mode of action. Ultraviolet (UV) radiation results in aphotochemical reaction that damages DNA and RNA molecules,inhibiting their replication and translation in cells (Newman, 2004).The peak of UV absorbance by DNA is at 260 nm (Hijnen et al.,2006) which is within the UVc range of 100–280 nm (Diffey, 2002).UVc radiation systems consist of low or medium pressure mercurylamps, a reactor (which is where the lamps are hold) and ballastor control box that regulates voltage (US-EPA, 1999). UVc radiationis often combined with other sanitizing options such as ozone oractivated peroxygens, leading to increased pathogen control.

2.2.2.2. Dose response. The effective range of UVc radiation to con-trol plant pathogens was between 28 mJ cm−2 for F. oxysporum f.sp. lycopersici (Runia, 1995) and 850 mJ cm−2 for Alternaria zinniae(Mebalds et al., 1996) (Table 9). The suggested water treatment forgrowers to control most pathogens is 250 mJ cm−2 (Runia, 1994b,1995).

2.2.2.3. Sensitivity to water chemistry and contaminants. Water andnutrient solution treated with UVc radiation must be low in tur-bidity to allow at least 60% transmission (Yiaosumi et al., 2005).Therefore, filtration should precede UVc radiation to prevent inter-ference of absorbance by suspended solids (Newman, 2004; Runia,1995; Stanghellini et al., 1984). In a survey of dam and runoffwater samples from 29 plant nurseries in Australia, less than athird of nurseries had high enough clarity for UV transmission tobe an effective water treatment method, even after filtration to5 �m (James et al., 1996). Higher UVc radiation intensities wererequired to achieve the same pathogen mortality in nutrient solu-tions compared with clear water (Sutton et al., 2009). The ironcontent (specific form was not indicated) in a hydroponic nutri-ent solution was reduced from 4.5 to 0.1 �g L−1 after being treatedwith UVc radiation at 30 mJ cm−2 (Stanghellini et al., 1984), and UVlight can lead to photo-degradation of iron chelates (Albano andMiller, 2001). Because UVc radiation is a physical water treatment,its efficacy is not pH dependent (Stewart-Wade, 2011).

2.2.2.4. Regulation. Radiation with UV is a point treatment with noresidual effect or toxic byproducts (Wolfe, 1990; Stewart-Wade,2011).

2.2.3. Heat treatment2.2.3.1. Mode of action. High temperatures disrupt cell integrityand interrupt metabolic processes in sensitive microorganisms
(Crisan, 1973). Heat treatment is applied by passing water througha series of heat exchangers until the target temperature is reached.After the required contact time is provided, heat is recovered andthe irrigation solution is cooled before application to the crop


Table 7Efficacy of bromine for control of waterborne plant pathogens.

Organism (life stage) Treatment dose(mg L−1, contact time)

Percentagecontrol (%)


Algae (unidentified) 15 mg L−1 (first 5weeks) and 30 mg L−1

(final 9 weeks)

4a Not observed Ficus benjamina, Scheffleraarboricola and Dieffenbachiamaculata

Chase andConover (1993)

Alternaria panax 50–60 mg L−1, dailyirrigation

82% Not observed Brassaia actinophylla Chase (1991)

Alternaria panax 50–60 mg L−1, dailyirrigation

90% Not observed Polyscias fruticosa Chase (1991)

Botrytis cinerea 50–60 mg L−1, dailyirrigation

15% (flowers),3% (leaves)

Not observed Pelargonium hortorum Chase (1991)

Botrytis cinerea 50–60 mg L−1, dailyirrigation

0% White spots on flowers Saintpaulia ionantha Chase (1991)

Corynespora cassiicola 50–60 mg L−1, dailyirrigation

93% Distortion of immature leavesand abscission with severenecrosis

Aeschynanthus pulcher Chase (1991)

Drechslera setariae 50–60 mg L−1, dailyirrigation

71% Not observed Maranta leuconeura Chase (1991)

Erwinia chrysanthemi 55 mg L−1, dailyirrigation

71 or 80%b,c Not observed Philodendron selloum Chase (1990)

Erwinia chrysanthemi 55 mg L−1, dailyirrigation

100%d Not observed Philodendron selloum Chase (1990)

Fusarium moniliforme 50–60 mg L−1, dailyirrigation

80% Chlorotic tip burn on olderleaves

Dracaena marginata Chase (1991)

Myrothecium roridum 50–60 mg L−1, dailyirrigation

77% Chlorotic etching on immatureleaves

Ficus pumila Chase (1991)

Myrothecium roridum 50–60 mg L−1, dailyirrigation

0% Not observed Syngonium podophyllum Chase (1991)

Pseudomonas andropogonis 25 mg L−1, dailyirrigation

0 or 59%b Not observed Bougainvillea sp. Chase (1990)

Pseudomonas cichorri 25 mg L−1, dailyirrigation

71% Not observed Chrysanthemum morifolium Chase (1990)

Pseudomonas cichorri 55 mg L−1, dailyirrigation

100% Not observed Chrysanthemum morifolium Chase (1990)

Pseudomonas syringae 25 mg L−1, dailyirrigation

60 or 70%b Not observed Impatiens wallerana Chase (1990)

Rhizoctonia solani 50–60 mg L−1, dailyirrigation

88 Not observed Epipremnum aureum Chase (1991)

Rhizoctonia solani 50–60 mg L−1, dailyirrigation

93% Not observed Nephrolepis exaltata Chase (1991)

Xanthomonas campestris pv.dieffenbachiae

55 mg L−1, dailyirrigation







40% Not observed Anthurium andraeanum Chase (1990)



12% Not observed Dieffenbachia maculata Chase (1990)

Xanthomonas campestris pv.fici


55% Observed (symptoms notspecified)

Ficus benjamina Chase (1990)

Xanthomonas campestris pv.fici


0 or 60%b Not observed Ficus benjamina Chase (1990)

Xanthomonas campestris pv.hederae


46 or 88% Observed (symptoms notspecified)

Hedera helix Chase (1990)

Xanthomonas campestris pv.hederae


87% Not observed Hedera helix Chase (1990)

Xanthomonas campestris pv.malvacearum


100% Observed (symptoms notspecified)

Hibiscus rosa-sinensis Chase (1990)

Xanthomonas campestris pv.malvacearum


76% Not observed Hibiscus rosa-sinensis Chase (1990)

Xanthomonas campestris pv.pelargonii


67 or 70% Not observed Pelargonium hortulanum Chase (1990)

a Rated in a 5 point scale where 1 = none, white bench, and 5 = complete green surface.

(mto

2h

b Results from two separate experiments.c Under high disease pressure.d Under low disease pressure.

Stewart-Wade, 2011; Van Os, 2010). Heat treatment is more com-only used to control microorganisms in greenhouses in Europe

han in the United States, probably because of European restrictions
n chemical use (Runia and Amsing, 2001; Van Os, 2010).
.2.3.2. Dose response. Effective control of plant pathogens witheat treatment ranged from 40 ◦C for 90 s for Phytophthora

cryptogea zoospores (Runia and Amsing, 2001) to 95 ◦C for 30 s forAgrobacterium tumefaciens (Poncet et al., 2001) (Table 10).

2.2.3.3. Sensitivity to water chemistry and contaminants. Heat gen-erally has little interaction with the nutrient solution and doesnot result in toxic chemicals (Runia, 1995). However, scale (saltprecipitates) may clog the irrigation system.


Table 8Efficacy of filters for removal of waterborne microorganisms.

Organism (life stage) Pore size Flow rate Material Propagulesremoved (%)

Crop References

Pythium myriotylum (zoospores) 0.5 �m prefilteredwith 1.0 �m

20 L min−1 Polypropylenemembrane

88%a Capsicumannuum

Schuerger and Hammer (2009)

Pythium aphanidermatum(zoospores)

20 �m 57 L min−1 Cartridge filter 67%a Cucumis sativus Goldberg et al. (1992)

Pythium myriotylum (zoospores) ≥1.0 �m 20 L min−1 Polypropylenemembrane

44%a Capsicumannuum

Schuerger and Hammer (2009)


7 �m prefilteredwith 20 �m

57 L min−1 Membrane cartridge 100%a Cucumis sativus Goldberg et al. (1992)

Cylindrocladium candelabrum 0.05 �m 40 mL min−1 Fiber polymericultrafiltration

100% None Machado et al. (2013)

Globodera rostochiensis,Meloidoigyne incognita,Radopholus similis

1 �m prefilteredwith 1 �m, 80 �mand 150 �m

17 L min−1 Polyester felt filter bags(1, 80 �m)

100% None Moens and Hendrickx (1992)

Metal gauze cartridge(150 �m)


5 �m 50 L min−1 Fiber membranestrands

100% In vitro Tu and Hardwood (2005)


5 �m 50 L min−1 Celllulose polyester 100% In vitro Tu and Hardwood (2005)

Botrytis cinerea 0.05 �m 40 mL min−1 Fiber polymericultrafiltration


Pseudomonas solanacearum 0.3 �m prefilteredwith 10 �m

27 L min−1 Poly-sulphone 99% In vitro Ohtani et al. (2000)

Ralstonia solanacearum 0.05 �m 40 mL min−1 Fiber polymericultrafiltration


Xanthomonas axonopoid 0.05 �m 40 mL min−1 Fiber polymericultrafiltration


Globodera rostochiensis,Meloidoigyne incognita,Radopholus similis

3 �m prefilteredwith 5 �m and150 �m

Not specified Polypropylene filterbags (3, 50 �m)

97% None Moens and Hendrickx (1992)

Metal gauze cartridge(150 �m)

a Reduction in disease incidence.

Table 9Efficacy of ultraviolet radiation for control of waterborne microorganisms.

Organism (life stage) Treatment dose (mJ cm−2) Inactivatedpropagules (%)

Crop References

Agrobacterium tumefaciens 71 mJ cm−2 15% Rosa sp. Poncet et al. (2001)Alternaria zinniae (spores) 850 mJ cm−2 100% In vitro Mebalds et al. (1996)Colletotrichum capsici (spores) 31 mJ cm−2 100% In vitro Mebalds et al. (1996)Fusarium oxysporum f. sp.

lycopersici (conidia)28 mJ cm−2 92% Solanum

lycopersicumRunia (1994b)

Fusarium oxysporum f. sp.lycopersici (conidia)

28 mJ cm−2 80% Rosa sp. Runia (1994b)

Fusarium oxysporum f. sp.melongenae (conidia)

50 mJ cm−2 96% Solanum melongena Runia (1994b)

Fusarium oxysporum (spores) 30 mJ cm−2 100% In vitro Mebalds et al. (1996)Fusarium oxysporum f. sp.

chrysanthemi (conidia)300 mJ cm−2 100% a Gerbera sp. Minuto et al. (2008)

Fusarium oxysporum f. sp.cyclaminis (conidia)

45 mJ cm−2 (water) 45 mJ cm−2

(nutrient solution)99.4% In vitro Sutton et al. (2009)

75%Phytophthora cinnamomi

(spores)43 mJ cm−2 100% In vitro Mebalds et al. (1996)

Pythium aphanidermatum 30 mJ cm−2 100% Spinacia oleracea Stanghellini et al. (1984)Pythium aphanidermatum 88 mJ cm−2 50% In vitro Tu and Zhang (2000)Pythium aphanidermatum

(zoospores)45 mJ cm−2 >99.9% (water) In vitro Sutton et al. (2009)

<90% (nutrient solution)Pythium aphanidermatum

(zoospores)17 mJ cm−2 (water) 100% In vitro Sutton et al. (2009)

38 mJ cm−2 (nutrient solution)Pythium aphanidermatum

(zoospores)20 mJ cm−2 99% In vitro Tu and Zhang (2000)

Pythium ultimum (spores) 40 mJ cm−2 100% In vitro Mebalds et al. (1996)ToMV 118 mJ cm−2 97%b Cucumis sativus Runia (1994b)ToMV 100 mJ cm−2 99%b Solanum melongena Runia (1994b)

a Disease incidence.b Reduction in lesions caused by virus.


Table 10Efficacy of heat treatment for control of waterborne microorganisms.

Organism (life stage) Treatment (time, contact time) Inactivated propagules (%) References

Agrobacterium tumefaciens 95 ◦C, 30 s 100% Poncet et al. (2001)Erwinia chrysanthemi 54 ◦C, 15 s; 99.80% Runia and Amsing (2001)

50 ◦C, 110 s; or 46 ◦C, 300 sErwinia chrysanthemi 42 ◦C, 110 s 30% Runia and Amsing (2001)Fusarium oxysporum f.sp. lycopersici (conidia) 54 ◦C, 15 s; or 100 Runia and Amsing (2001)

46 ◦C, 200 sPhytophthora cryptogea (zoospores) 44 ◦C, 15 s; or 100% Runia and Amsing (2001)

40 ◦C for 90 sPythium aphanidermatum (zoospores) 51 ◦C, 15 s; or 100% Runia and Amsing (2001)

47 ◦C, 45 sRadopholus similis 49 ◦C for 15 s 100% Runia and Amsing (2001)

◦

2

22pfisma(W1ltStWtwoataahfrb1

2obcVeashp(c1

2fics

ToMV 95 C for 10 s

ToMV 85 ◦C for 3 min

Verticillium dahliae 90 ◦C, 10 s

.3. Ecological water treatments

.3.1. Slow sand filtration

.3.1.1. Mode of action. Slow sand filtration controls plantathogens by biological, physical and chemical reactions. Slow sandlters are composed of sand, gravel, and underdrainage pipes. Theand in slow sand filtration systems, unlike in rapid sand filters,ust be homogeneous, fine (<0.3 mm diameter) and round (Ellis

nd Wood, 1985). Media other than sand have been evaluatedWohanka et al., 1999), but are typically not used commercially.

ater flows slowly through layers of fine sand at a rate between00 and 300 L m−2 h−1 (Wohanka, 1995), through a height of at

east 1.4 m to allow prolonged contact time. An upper layer onhe sand bed contains a complex microbial community, known aschmutzdecke, which carries out biological control in slow sand fil-ration by a mechanism that remains to be characterized (Ellis and

ood, 1985; Gimbel et al., 2007). Therefore, in slow sand filtra-ion systems, the upper layer of sand must always be covered withater to maintain the microbial population responsible for control

f pathogens. Biological control of microbes can occur either by par-sitic interactions or by the release of antimicrobial metabolites orhe combination of both (Weller et al., 2002). Slow sand filtrationlso removes pathogens by physically entrapping the pathogensnd debris that carry pathogens. A lower 0.5 m deep layer of gravelelps maintain the structure of the filter by separating the sand

rom the underdrainage. The underdrainage is a series of perfo-ated pipes that holds the filter and also helps maintain water flowy draining the water from the filter to a reservoir (Ellis and Wood,985).

.3.1.2. Efficiency of removal. Slow sand filtration has beenbserved to remove a high percentage of Phytophthora, Fusarium,acteria, nematodes, and viruses from irrigation water, but may notompletely eliminate them (Ufer et al., 2008; Lee and Oki, 2013;an Os et al., 1999; Van Os, 2010; Wohanka, 1995) (Table 11). Thefficiency of slow sand filtration depends on the media materialnd the depth of the filter (Wohanka et al., 1999). A compari-on of different filter media showed that rockwool media had theighest (99%) removal efficiency of Xanthomonas campestris pv.elargonii compared with sand (83%), pumice (85%) and anthracite82%). Rockwool filters with depths of 60 or 90 cm removed more X.ampestris pv. pelargonii than a 30 cm depth filter (Wohanka et al.,999).

.3.1.3. Sensitivity to water chemistry and contaminants. Slow sandltration does not alter the concentration of elements, pH or electri-al conductivity of the nutrient solution (Wohanka, 1995). Becauselow sand filtration is a type of biological control treatment, any

100% Runia (1995)100% Runia and Amsing (2001)

94% Runia (1995)

factor (such as temperature or pH) that affects the biology ofmicroorganisms will affect the activity in the Schmutzdecke.

2.3.2. Biosurfactants2.3.2.1. Mode of action. Rhamnolipid and nitrapyrin are two bio-surfactants evaluated for use as water treatment. Rhamnolipidbiosurfactant is a contact biofungicide that is produced from theaerobic fermentation of Pseudomonas aeruginosa (Stanghellini andMiller, 1997; US-EPA, 2013b). Rhamnolipids disrupt cells mem-branes of oomycetes, with zoospores being the most vulnerable lifestage (US-EPA, 2013b). Nitrapyrin is an active ingredient of nitrifi-cation inhibitor products, which in a recirculated solution increasedthe populations of beneficial bacteria (Pseudomonas putida) whilereducing oomycete survival and disease incidence (Pagliaccia et al.,2007). Nitrapyrin is labeled as a nitrogen stabilizer only and is notlabeled as a pesticide.

2.3.2.2. Dose response. Continuous application of 150 mg L−1 ofrhamnolipid controlled 100% of disease caused by P. capsici in pep-per plants (Capsicum annuum) (Table 12). Nutrient solution treatedwith nitrapyrin resulted in 40% less mortality of cucumber plants(Cucumis sativus) caused by P. aphanidermatum than untreated con-trol (Pagliaccia et al., 2007). Nutrient solutions of pepper plantstreated with rhamnolipid and nitrapyrin biosurfactant resulted intwo orders of magnitude higher concentration of aerobic bacte-ria (Nielsen et al., 2006) and P. putida (Pagliaccia et al., 2007) thanthe untreated solution. Proliferation of beneficial bacteria may bea secondary benefit of using biosurfactants, however high bacte-rial density also increases the risk of biofilm buildup and irrigationemitter clogging (Rogers et al., 2003).

2.3.2.3. Phytotoxicity. Reduction in plant biomass of pepper plantswas observed when 150 mg L−1 rhamnolipid biosurfactant whenapplied in overhead and ebb and flow irrigation in organic or rock-wool media (Nielsen et al., 2006). Nitrapyrin at 12.5 mg L−1 reducedplant growth of peppers and resulted in chlorosis (Pagliaccia et al.,2007).

2.3.2.4. Regulation. No adverse health effects, except eye irrita-tion, have been observed with the use of rhamnolipid biosurfactant(US-EPA, 2013b). Because of the low concentration of active ingre-dient and fast degradation in the environment, minimal toxicityfrom the residual concentrations in runoff is expected (US-EPA,2013b).

2.3.3. Constructed wetlands2.3.3.1. Mode of action. The mechanism by which constructedwetlands remove pathogens is most likely through complex andinteracting physicochemical and biological processes within the


Table 11Efficacy of slow filtration for control of waterborne microorganisms.

Material Organism (life stage) Propagules removed (%) References

Antracite Xanthomonas campestris pv.pelargonii

Antracite, grain size 0.8–1.6 mm at a flow rate of 200 L m−2 h−1

removed 82% of Xanthomonas campestris pv. pelargonii from a nutrientsolution.

Wohanka et al. (1999)

Lava grain Phytophthora spp. Slow sand filtration at a flow rate between 566 L m−2 h−1completelyremoved Phytophthora spp. from commercial nursery runoff.

Ufer et al. (2008)

Pumice Xanthomonas campestris pv.pelargonii

Pumice grain size 0.4–4 mm at a flow rate 200 L m−2 h−1 removed 85%of Xanthomonas campestris pv. pelargonii from nutrient solution.


Rockwool Xanthomonas campestris pv.pelargonii

Rockwool granulate at a density of 136 kg m−3 at a flow rate200 L m−2 h−1 removed 99% of Xanthomonas campestris pv. pelargoniifrom nutrient solution.


Sand Fusarium oxysporum f.sp.chrysanthemi (conidia)

Slow sand filtration at a flow rate of 200 L m−2 h−1 reduced 89% of theincidence of Fusarium wilt on Gerberas.

Minuto et al. (2008)

Sand Fusarium oxysporum f.sp.cyclaminis

Slow sand filtration with an effective surface of 279 cm−2 at a flow rateof 200 L m−2 h−1 reduced the concentration of Fusarium oxysporum f.sp. cyclaminis in >99.9%.

Wohanka (1995)

Sand Pelargonium flower break virus Slow sand filtration (200 L m−2 h−1, area 279 cm2) reduced around 70%of Pelargonium flower break virus and viral infection in geraniumsfrom nutrient solution.

Berkelmann et al. (1995)

Sand Phytophthora spp. Slow sand filtration at a flow rate between 269 and 300 L m−2 h−1

completely removed Phytophthora spp. from commercial nurseryrunoff.

Ufer et al. (2008)

Sand Phytophthora capsici Slow sand filtration at a flow rate of 148 L m−2 h−1 in a 2 m long filterremoved 100% of Phytophthora capsici from week 2 to 5.

Lee and Oki (2013)

Sand Phytophthora capsici Slow sand filtration at a flow rate of 148 L m−2 h−1 in a 2 m long filterdid not removed Fusarium oxysporum from week 2 to 5.

Lee and Oki (2013)

Sand Phytophthora cinnamomi Slow sand filtration (sand grain size between 0.15 and 0.35 mm with adiameter of 15 cm and depth of 80 cm) at a filtration rate of100 L m−2 h−1 removed 100% of Phytophthora cinnamomi from nutrientsolution.

Van Os et al. (1999)

Sand Phytophthora cryptogea(zoospores)

After week 3 of the establishment of the slow sand filtration system,100% removal of Phytophthora cryptogea zoospores was observed.

Calvo-Bado et al. (2003)

Sand Radopholus similis Slow sand filtration (sand grain size between 0.2 and 0.8 mm with adiameter of 15 cm and depth of 80 cm) at a filtration rate of100 L m−2 h−1 removed 96% of Radopholus similis from nutrient

ys.

Van Os et al. (1999)

(graipestr

wwkcoem

TE

solution after 21 daSand Xanthomonas campestris pv.

pelargoniiSlow sand filtrationof Xanthomonas cam

etland ecosystem (Headley et al., 2005; Huett, 2002). Constructedetlands used to treat agricultural runoff can be surface-flow (also

nown as free-water surface), subsurface-flow (horizontal or verti-
al flow), or a combination of both (White et al., 2011). Surface flowr free water surface wetlands consist of a shallow basin with veg-tation (typically perennial grasses) that allow effluent to slowlyove above the soil surface. Water flows through the wetland for
able 12fficacy of biosurfactants for control of waterborne microorganisms.

Active ingredient Organism (lifestage)

Treatment dose(mg L−1, contact time)

Inactivatedpropagules (%)

Nitrapyrin Phytophthoracapsici (zoospores)

12.5 mg L−1,a 69%b

Nitrapyrin Pythiumaphanidermatum(mycelia)

12.5 mg L−1,a 46%b

Nitrapyrin Pythiumaphanidermatum(mycelia)

12.5 mg L−1,a 40%c

Rhamnolipid Phytophthoracapsici (zoospores)

150 mg L−1, continous 100%

Rhamnolipid Phytophthoracapsici (zoospores)

60 mg L−1, <10 s 100%

Rhamnolipid Plasmoparalactucae-radicis(zoospores)

60 mg L−1, <10 s 100%

Rhamnolipid Pythiumaphanidermatum(zoospores)

60 mg L−1, <10 s 100%

a Single application in agar media.b Reduction in mycelia growth.c Reduction in plant mortality.

n size 0.2–2 mm, depth 80 cm) removed 93%is pv. pelargonii


approximately three days and finally the water is released to areservoir for reuse (White et al., 2011). Flow rate in and out ofthe wetland is managed to promote interaction with plant roots
and microbes in the environment (Vymazal, 2005). In contrast, insubsurface-flow wetlands aquatic plants are planted on a mediabed (typically gravel or clay) and the effluent moves through thelayer of media (Vymazal, 2005).

N/A In vitro Pagliaccia et al. (2007)

N/A In vitro Pagliaccia et al. (2007)

Reduction inbiomass, chlorotic

Cucumis sativus Pagliaccia et al. (2007)

Reduction inbiomass

Capsicum annuum Nielsen et al. (2006)

N/A In vitro Stanghellini and Miller (1997)



R.E. Raudales et al. / Agricultural Wate

Table 13Number of citations found for efficacy studies on control waterborne microorgan-isms for a range of water treatment technologies.a

Water treatment Genus Species In vitro References

Biosurfactants 3 3 2 3Bromine 10 13 0 3Chlorine 16 27 13 20Chlorine dioxide 15 15 7 9Copper ions from

electrolysis11 12 1 12

Copper ions from dissolvedsalts

4 10 4 6

Heat 8 8 0 3Hydrogen peroxide and

peroxyacetic acid10 10 4 7

Membrane filters 3 4 2 5Ozone 9 9 4 6Silver ionization 0 0 0 0Silver salts 5 6 1 1Slow sand filtration 5 6 0 8

2l(of(la

2sfce2re

3

smaufaceetcdwo2wcb1T

cet

Ultraviolet light 7 8 3 7

a Literature review carried out in December, 2013.

.3.3.2. Efficiency of removal. A subsurface-flow constructed wet-and with a surface of 4 m2 and 0.5 m deep planted with reedPhragmites australis) in a gravel bed was effective in removing 100%f the inoculated Phytophthora cinnamomi in a retention time (timerom inflow to outflow) of 1.3 and 4.5 days throughout the yearHeadley et al., 2005; Huett, 2002). The efficacy of constructed wet-ands to control waterborne pathogens is an active and emergingrea of research.

.3.3.3. Sensitivity to water chemistry and contaminants. Con-tructed wetlands are highly effective in removing contaminantsrom runoff and sewage (Vymazal, 2009; White et al., 2011). In agri-ulture, constructed wetlands are known for their high removalfficacy (≥80%) of total nitrogen and phosphorus (Headley et al.,005; White et al., 2011). Adequate timing in the harvesting andeplacement of the plants is crucial for proper absorption of nutri-nts (Headley et al., 2005).

. Implications for research and effective water treatment

Experimental efficacy trial results provide only one aspect in theelection of dosage levels and successful design of a water treat-ent system. Additional factors that interact in real life scenarios

t grower operations are usually excluded from research conductednder controlled conditions. Irrigation management is impacted byactors such as the water source, flow rates and volume, temper-ture, organic and inorganic contaminants, pH, irrigation systemomponent materials, crop sensitivity to phytotoxicity, and socio-conomic considerations such as capital and operating costs. Mostfficacy research has been carried out in vitro (Table 13), and addi-ional research is needed under environments that resemble theonditions of actual operations. Efficacy to control microbes greatlyiffered when evaluations were conducted in pure water comparedith nutrient solutions (Sutton et al., 2009; Vanachter et al., 1988)

r in vitro compared with in vivo conditions (Gracia-Garza et al.,002). Most efficacy testing has focused on pathogen mortality,hereas disease development is most important to commercial

rop production, and experiments have observed discrepanciesetween pathogen mortality and disease incidence (Datnoff et al.,987; Schuerger and Hammer, 2009; Stanton and O’Donnell, 1994;u and Hardwood, 2005).

For resistant pathogens, the required water treatment con-entration may exceed the threshold for crop phytotoxicity. Forxample, doses above 4 mg L−1 chlorine were required to con-rol several pathogens in water (Cayanan et al., 2009a; Chase and

r Management 143 (2014) 9–28 23

Conover, 1993; Hong et al., 2003; Poncet et al., 2001; Rav-Acha et al.,1995; Rosner et al., 2006; Stanton and O’Donnell, 1994), whereasthe identified phytotoxicity threshold was 2.4 mg L−1 (Cayananet al., 2009b) (Fig. 1). Similar patterns were observed with ozone,copper, bromine and hydrogen peroxide. Therefore, a challengefor practitioners is to apply an effective dose for microbial controlwhile minimizing risk of phytotoxicity. The phytotoxicity thresholdfor most crops and sanitizing agents remains to be established. Incases where pathogens are highly resistant to chlorination, such asFusarium, viruses and nematodes (Fig. 1), other water treatmentsshould be selected, or other integrated pest management meth-ods (such as pesticide applications directly to the crop, use of cleanplant material, and sanitation of surfaces) are necessary. The over-all design of a water treatment system should be driven by plantpathology research findings on required dosage and contact times,potentially utilizing holding tanks or baffled flow to increase con-tact time. If a high treatment concentration is applied, research isneeded on removal of active ingredient level to below the phy-totoxicity threshold before water reuse, through aeration, carbonfiltration, or other technologies.

The selection of water treatments is a difficult task for growers,particularly given the large selection of options available, and thelimited and variable knowledge about efficacy (Table 13). Despitethe number of review articles discussing the available water treat-ment options and their technical characteristics (Ehret et al., 2001;Newman, 2004; Raviv and Lieth, 2007; Runia, 1995; Van Os, 2010;Stewart-Wade, 2011; Zhou and Smith, 2002), the literature lacksclear guidelines for selecting a technology. Growers are willing toadopt risk management strategies, such as water treatment, to pre-vent plant disease spread in their operations (Breukers et al., 2012).With new regulations pending to reduce the risk of water-bornecontamination of fresh produce by human pathogens (US-FDA,2013) there will be an even greater need to provide growers withthe tools they need to make informed choices. However, risk anduncertainty are major factors that prevent adoption of innovationsin agriculture (Feder and Umali, 1993; Marra et al., 2003). Withvery limited research data, as evidenced by the small number ofstudies for most water treatments other than chlorine and copper(Table 13), growers must make decisions despite major knowl-edge gaps. The authors have provided published efficacy data in asearchable online database (“Waterborne Solutions” at watereduca-tionalliance.org) to improve access to the existing knowledge base.

Adoption of innovations in agriculture requires considerationof socioeconomic factors other than the technology itself, includ-ing operation size, adaptability to current infrastructure, perceivedtechnical benefits, ease of use, costs, financial benefits, externalincentives, and public policy among others (Adesina and Zinnah,1993; Feder and Umali, 1993; Loo et al., 2012; Mangiafico et al.,2008; Rogers, 2003). A preliminary survey of water treatment costin U.S. greenhouse operations (Raudales, 2013) found a wide rangein treatment cost (from $US0.02 per m3 for chlorination via calciumhypochlorite, sodium hypochlorite, or chlorine gas up to $US5.15per m3 for one brand of chlorine dioxide treatment). For the watertreatments listed in Table 13, ionized copper and silver, heat, mem-brane filters, ozone, slow sand filtration, constructed wetlands,and UV light are more capital intensive than injectable chemi-cals such as biosurfactants, bromine, chlorine, chlorine dioxide,and copper salts. Capital-intensive technologies are therefore morelikely to be suitable for large water volumes where economies ofscale reduce the capital cost per volume treated. Belayneh et al.(2013) described a case study in Tennessee, where the cost of thewell water supply ($US0.045 per m3) was a consideration when
evaluating return on investment in sensor-based irrigation tech-nology. Raudales (2013) found that the cost of water supply forseveral greenhouse operations in the U.S. varied between $US0.02to $US1.62 per m3 depending on the water supply and local costs,


Agrobacterium

Algae

Ralstonia Xanthomonas

Virus

Fusarium

Nematodes

Phytophthora (zoospores)

Pythium

0 mg/L

≥ 4 mg/L

1 mg/L

2 mg/L

3mg/L

Botry�sErwinia

Rhizoctonia

Phytophthora(other life stages)

Geotrichum Chlamydomonas

Chlorella

Microphorimidum

Reported Phytotoxicity

nd phy

aeiqrcoc

rtbaasctad1

ssdaectwic2ncatrct

Fig. 1. Summary of reported efficacy a

nd that in cases where water soluble fertilizer was used, nutri-nts added between $US0.23 to $US1.30 per m3 to the price of anrrigation solution. More detailed economic analysis is needed touantify return on investment in water capture, treatment, andeuse, including quantification of costs of the water source, recir-ulation system design including water flow and treatment, andther benefits such as reduced crop losses from pathogens or laborosts from clogged emitters.

Although water treatment is a risk management strategy, theisk of waterborne pathogens has yet to be clearly quantified inhe complex environment of commercial operations. This includesoth the required inoculum level for infection in irrigation water,nd also a risk analysis of inoculum sources including incomingnd recirculated water, potting substrate, plant material, and otherources. Parke and Grünwald (2012) used a hazard analysis ofritical control points (HACCP) analysis to identify points of con-amination with Phytophthora ramorum in plant nurseries. A HACCPpproach has also been used to identify sources of contamination inrinking water sources, distribution systems and storage (Havelaar,994).

Horticultural operations that recirculate water are effectivelymall-scale water treatment plants similar to municipal drinkingupply facilities, with the associated need for holistic design, redun-ancy in treatment, and standardized protocols for maintenancend monitoring. A multi-barrier approach that incorporates sev-ral treatment technologies focused on critical control points isommonly used for risk management in drinking- and waste-waterreatment. The concept of multi-stage water treatment in drinkingater has a long history (Galvis, 2002), and has equal importance

n horticulture applications where physical, chemical, and ecologi-al treatments can and should be combined (Lewis Ivey and Miller,013). Multiple stages of filtration is an underlying design compo-ent, in order to reduce the amount of inoculum that needs to behemically treated as well as removing organic matter that creates

sanitizing agent demand. Water treatments in Table 13 vary in
heir modes of action, as described in Section 2, and also in theiresidual effect. Biosurfactants, bromine, chlorine, chlorine dioxide,opper, hydrogen peroxide, and silver have residual effects throughhe irrigation system, whereas filtration, heat, slow sand filtration,
totoxicity of chlorine-based products.

UV light are point treatments within the irrigation flow, and highly-reactive ozone also has limited residual. Combining point andresidual treatments may provide an initial disinfestation followedby continued control throughout the irrigation system. Research inthe design and performance of entire treatment systems is needed,particularly because some currently installed systems are unableto control microbial load to target levels (Meador et al., 2012).

Because inoculum load varies over time in irrigation systems,monitoring is a critical component in order to reduce risk of dis-ease as consequence of under-dosing, or the risk of phytotoxicity,worker hazard, and increased cost from over-dosing. Kits for onsitemeasuring of active ingredient are available for chlorine, chlorinedioxide, copper, activated peroxygens and ozone. Onsite tests ofmicrobial load in irrigation water (Meador et al., 2013), and dis-ease testing by clinical laboratories are available. However, basedon an evaluation of management practices at commercial groweroperations (Meador et al., 2012), more training and emphasis onmonitoring are needed or water treatment will be an unreliablerisk management strategy.

Effective water treatment for irrigation must adapt to vary-ing conditions in water temperature and water chemistry (suchas pH and oxidation–reduction potential) which fluctuate season-ally and diurnally in irrigation ponds (Hong et al., 2009). At lowerwater temperatures, survival of Phytophthora spp. spores is pro-longed (Porter and Johnson, 2004), but the overall concentrationof pathogens is typically lower compared with higher tempera-tures (Bates and Stanghellini, 1984; Bush et al., 2003; Gevens et al.,2007). Water temperature can also affect pathogen species compo-sition. For example, P. aphanidermatum predominated above 23 ◦Cin a hydroponic spinach operation, whereas P. dissotocum predom-inated at a cooler temperature (Bates and Stanghellini, 1984). Thisvariable microbial load in irrigation water further emphasizes theneed for monitoring.

Organic matter in the water reduces residual concentrationof sanitizing agents, and filtration underlies subsequent treat-
ment. Surface water sources tend to have higher microbialconcentrations and suspended solids than well and municipalwater (Cappaert et al., 1988; Meador et al., 2012; Pottorff andPanter, 1997). Research evaluating the effect of organic matter on

Wate

srpcyIbobtiopiJis

4

ibsrot

wroahciih

ctmcciipth

A

taEf

R

A

A

AA

R.E. Raudales et al. / Agricultural

anitizer demand indicated that the residual concentration of chlo-ine and chlorine dioxide significantly decreased (>53%) by theresence of 50 mg L−1 peat in suspension; whereas the residualoncentration of ionized copper, copper salts and activated perox-gens were minimally affected by peat (<5.5%) (Fisher et al., 2013).n drinking and waste-water management, the degree of requirediological treatment is determined by estimating the concentrationf organic matter (Maier et al., 2009). Organic matter in solution cane estimated by measuring biochemical oxygen demand (indicateshe amount of oxygen consumed by heterotrophic bacteria), chem-cal oxygen demand (indicates the amount of oxygen necessary toxidize organic carbon in the solution) or total organic carbon. Theersistence of plant pathogens (Phytophthora spp.) can increase

n the presence of suspended soil in irrigation water (Porter andohnson, 2004). Monitoring the concentration of organic mattern the irrigation water will help determine the necessary appliedanitizing agent concentration.

. Conclusions

Irrigation water treatment is a risk management strategy aim-ng to reduce economic losses associated with plant pathogens,iofilms, and algae. This summary of efficacy tests is intended toupport agricultural management decisions, by indicating the cur-ent state of knowledge on effective dose for controlling targetrganisms under research conditions, in addition to reported phy-otoxicity thresholds.

There are widely varying levels of knowledge of the differentater treatment options for irrigation (Table 13). Although chlo-

ine and copper ionization have been studied by several researchersn different microorganisms, other non-chemical options suchs slow sand filters, constructed wetlands, and membrane filtersave received less research effort. Limited research has also beenonducted on effective control methods for algae and biofilmsn horticultural systems, which are common problems in micro-rrigation systems and result in plant loss, labor costs and workerazard.

Ultimately, water treatment is just one component of integratedrop management. Research summaries in Tables 1–12 showedhat target microorganisms vary widely in resistance to water treat-

ent. Application of one water treatment technology may notontrol resistant pathogens without risk of phytotoxicity or excessost, and will not control potential sources of inoculum other thanrrigation water. Selection of resistant cultivars, disease-free start-ng plant material, monitoring of water quality, matching irrigationractices with plant water need, preventive applications of pes-icides, are just some of the management practices essential forealthy and safe crops (Jarvis, 1992).

cknowledgements

We thank the USDA-ARS Floriculture and Nursery Research Ini-iative, and industry partners of the Floriculture Research Alliancet the University of Florida (floriculturealliance.org) and Waterducation Alliance for Horticulture (watereducationalliance.org)or supporting this research.

eferences

desina, A.A., Zinnah, M.M., 1993. Technology characteristics, farmer’s perceptionsand adoption decisions: a Tobit model application in Sierra Leone. Agr. Econ. 9,297–311.

din, A., Sacks, M., 1991. Dripper-clogging factors in wastewater irrigation. J. Irrig.Drain. Eng. 117 (6), 813–826.

grios, G., 2005. Plant Pathology, 5th ed. Elsevier Academic Press, San Diego, CA.lbano, J.P., Miller, W.B., 2001. Photodegradation of FeDTPA in nutrient solutions. I.

Effects of irradiance, wavelength, and temperature. HortScience 36 (2), 313–316.

r Management 143 (2014) 9–28 25

Amy, G., Bull, R., Gunther, G.F., Pegram, R.A., Siddiqui, M., 2000. Disinfectantsand Disinfectant by-products. World Health Organization, Geneva, Finland, pp.499, Retrieved on January 10, 2013 from: http://inchem.org/documents/ehc/ehc/ehc216.htm#SubSectionNumber:2.4.2

Baker, K.F., Matkin, O.A., 1978. Detection and control of pathogens in water. Orna-mentals Northwest Newslett. 2 (2), 12–14.

Bates, M.L., Stanghellini, M.E., 1984. Root rot of hydroponically grown spinach causedby Pythium aphanidermatum and P. dissotocum. Plant Dis. 68 (11), 989–991.

Beardsell, D., Bankier, M., 1996. Monitoring and Treatment of Recycled Water forNursery and Floriculture Production, Horticultural Australia Ltd. Final ReportNY515, Retrieved on January 10, 2013 from: http://www.ngia.com.au/Story?Action=View&Story id=1983

Belayneh, B.E., Lea-Cox, J.D., Lichtenberg, E., 2013. Cost and benefits of implementingsensor-controlled irrigation in a commercial pot-in-pot nursery. HortTechnol-ogy 23 (6), 760–769.

Benarde, M.A., Israel, B.M., Olivieri, V.P., Granstrom, M.L., 1965. Efficiency of chlorinedioxide as a bactericide. Appl. Microbiol. 13 (5), 776–780.

Berkelmann, B., Wohanka, W., Krezal, G., 1995. Transmission of Pelargonium flowerbreak virus (PFBV) by recirculating nutrient solutions with and without slowsand filtration. Acta Hortic. 382, 256–262.

Berry, D., Xi, C., Raskin, L., 2006. Microbial ecology of drinking water distributionsystems. Curr. Opin. Biotechnol. 17 (3), 297–302.

Bois, F.Y., Fahmny, T., Block, J.C., Gatel, D., 1997. Dynamic modeling of bacteria in apilot drinking water distribution system. Water Res. 31 (12), 3146–3156.

Bradford, K.J., Dilley, D.R., 1978. Effects of root anaerobiosis on ethylene productions,epinasty, and growth of tomato plants. Plant Physiol. 61 (4), 506–509.

Breukers, A., van Asseldonk, M., Bremmer, J., Beekman, V., 2012. Understandinggrowers’ decisions to manage invasive pathogens at the farm level. Phytopa-thology 102 (6), 609–619.

Bull, R.J., Gerba, C., Trussell, R.R., 1990. Evaluation of the health risks associated withdisinfection. Crit. Rev. Environ. Sci. Technol. 20 (2), 77–113.

Bush, E.A., Hong, C.X., Stromberg, E.L., 2003. Fluctuations of Phytophthora andPythium spp. in components of a recycling irrigation system. Plant Dis. 87 (2),1500–1506.

Calvo-Bado, L.A., Pettitt, T.R., Parsons, N., Petch, G.M., Morgan, J.A.W., Whipps, J.M.,2003. Spatial and temporal analysis of the microbial community in slow sandfilters used for treating horticultural irrigation water. Appl. Environ. Microbiol.69 (4), 2116–2125.

Camberato, D.M., Lopez, R.G., 2010. Commercial Greenhouse and Nursery Pro-duction: Controlling Algae in Irrigation Ponds, Purdue Extension publicationHO-247-W, Retrieved on January 10, 2013 from: http://www.extension.purdue.edu/extmedia/HO/HO-247-W.pdf

Cameron, A.C., Reid, M.S., 1983. Use of silver thiosulfate to prevent flower abscissionfrom potted plants. Sci. Hortic. 19 (3), 373–378.

Cappaert, M.R., Powelson, M.L., Franc, G.D., Harrison, M.D., 1988. Irrigation wateras a source of inoculum of soft rot Erwinias for aerial stem rot of potatoes.Phytopathology 78 (12), 1668–1672.

Carrillo, A., Puente, M.E., Bashan, Y., 1996. Application of diluted chlorine diox-ide to radish and lettuce nurseries insignificantly reduced plant development.Ecotoxicol. Environ. Saf. 35 (1), 57–66.

Cayanan, D.F., Zhang, P., Liu, W., Dixon, M., Zheng, Y., 2009a. Efficacy of chlorine incontrolling five common plant pathogens. HortScience 44 (1), 157–163.

Cayanan, D.F., Dixon, M., Zheng, Y., Llewellyn, J., 2009b. Response of container-grownnursery plants to chlorine used to disinfest irrigation water. HortScience 44 (1),164–167.

Chase, A.R., 1990. Control of some bacterial diseases of ornamentals with Agribrom.Proc. Fla. State Hortic. Soc. 103, 192–193.

Chase, A.R., 1991. Control of Some Fungal Diseases of Ornamentals with Agribrom,CFREC-Apopka Research Report, RH-91-3 Retrieved on January 10, 2013 from:http://mrec.ifas.ufl.edu/foliage/resrpts/rh 91 3.htm

Chase, A.R., Conover, C.A., 1993. Algae control in an ebb and flow irrigation system.Proc. Fla. State Hortic. Soc. 106, 280–282.

Cherney, D.P., Duirk, S.E., Tarr, J.C., Collette, T.W., 2006. Monitoring the speciation ofaqueous free chlorine from pH 1 to 12 with Raman spectroscopy to determinethe identity of the potent low-pH oxidant. Appl. Spectrosc. 60 (7), 764–772.

Choppakatla, V.K., 2009. Evaluation of SaniDate® 12.0 as a Bactericide, Fungicideand Algaecide for Irrigation for Irrigation Water Treatment. BioSafe Laboratory,Final Report 09-004.

Colburn, G.C., Jeffers, S.N., 2010. Efficacy of commercial algaecides to manage speciesof Phytophthora in suburban waterways. In: Sudden Oak Death Fourth ScienceSymposium, April 2010, pp. 223–224.

Cook, R.J., 2000. Advances in plant health management in the twentieth century.Annu. Rev. Phytopathol. 38 (1), 95–116.

Copes, W.E., Hendrix, F.F., 1996. Chemical disinfestation of greenhouse growingsurface materials contaminated with Thielaviopsis basicola. Plant Dis. 80 (8),885–886.

Copes, W.E., Chastaganer, G.A., Hummel, R.L., 2003. Toxicity responses of herbaceousand woody ornamental plants to chlorine and hydrogen dioxides. Online PlantHealth Prog., http://dx.doi.org/10.1094/PHP-2003-0311-01-RS.

Copes, W.E., Chastaganer, G.A., Hummel, R.L., 2004. Activity of chlorine dioxide in asolution of ions and pH against Thielaviopsis basicola and Fusarium oxysporum.
Plant Dis. 88 (2), 188–194.
Costerton, J.W., Lewandowski, Z., Caldwell, D.E., Korber, D.R., Lappin-Scott, H.M.,1995. Microbial biofilms. Annu. Rev. Microbiol. 49 (1), 711–745.

Crisan, E.V., 1973. Current concepts of thermophilism and the thermophilic fungi.Mycologia 65 (5), 1171–1198.

http://refhub.elsevier.com/S0378-3774(14)00183-8/sbref0005































































http://inchem.org/documents/ehc/ehc/ehc216.htm

http://inchem.org/documents/ehc/ehc/ehc216.htm






































http://www.ngia.com.au/Story?Action=View&Story_id=1983

































































































































































































http://www.extension.purdue.edu/extmedia/HO/HO-247-W.pdf

http://www.extension.purdue.edu/extmedia/HO/HO-247-W.pdf




















































































































http://mrec.ifas.ufl.edu/foliage/resrpts/rh_91_3.htm





































































































































dx.doi.org/10.1094/PHP-2003-0311-01-RS


















































2 Wate

D

D

D

D

DD

D

D

D

E

E

E

E

E

E

F

F

F

F

F

F

F

F

G

G

G

G

G

G

G

G

G

G

G


’Alessandro, A., Kuschner, W., Wong, H., Boushey, H.A., Blanc, P.D., 1996. Exagger-ated responses to chlorine inhalation among persons with nonspecific airwayhyperreactivity. Chest 109 (2), 331–337.

ate, S., Terabayashi, S., Kobayashi, Y., Fujime, Y., 2005. Effects of chloraminesconcentration in nutrient solution and exposure time on plant growth in hydro-ponically cultured lettuce. Sci. Hortic. 103 (3), 257–265.

atnoff, L.E., Kroll, T.K., Lacy, G.H., 1987. Efficacy of chlorine for decontaminatingwater infested with resting spores of Plasmodiophora brassicae. Plant Dis. 71 (8),734–736.

eborde, M., von Gunten, U., 2008. Reactions of chlorine with inorganic and organiccompounds during water treatment – kinetics and mechanisms: a criticalreview. Water Res. 42 (1), 13–51.

egrémont, S.A., 1979. Water Treatment Handbook. Halsted Press, New York, NY.ehghanisanij, H., Yamamoto, T., Ould Ahmad, B., Fujiyama, H., Miyamoto, K., 2005.

The effect of chlorine on emitter clogging induced by algae and protozoa andthe performance of drip irrigation. Trans. ASAE 48 (2), 519–527.

iffey, B.L., 2002. Sources and measurement of ultraviolet radiation. Methods 28 (1),4–13.

omingue, E.L., Tyndall, R.L., Mayberry, W.R., Pancorb, O.C., 1988. Effect of three oxi-dizing biocides on Legionella penumophila serogroup 1. Appl. Environ. Microbiol.54 (3), 741–747.

rechsler, C., 1952. Production of zoospores from germinating oospores of Pythiumultimum and Pythium debaryanum. Bull. Torrey Bot. Club 79, 431–450.

hret, D.L., Alsanius, B., Wohanka, W., Menzies, J.G., Utkhede, R., 2001. Disinfestationof recirculating nutrient solutions in greenhouse horticulture. Agronomie 21 (4),323–339.

l-Hamalawi, Z.A., 2007. Attraction, acquisition, retention and spatiotemporal dis-tribution of soilborne plant pathogenic fungi by shore flies. Ann. Appl. Biol. 152,169–177.

llis, K.V., Wood, W.E., 1985. Slow sand filtration. Crit. Rev. Environ. Control 15 (4),315–354.

lmer, W.E., 2008. Preventing spread of Fusarium wilt of Hiemalis begonias in thegreenhouse. Crop Prot. 27 (7), 1078–1083.

rwin, D.C., Ribeiro, O.K., 1996. Phytophthora Diseases Worldwide. APS, Press, St.Paul, MN, pp. 526.

vans, I., Solberg, E., Huber, D.M., 2007. Copper and plant disease. In: Datnoff, L.E.,Elmer, W.H., Huber, D.M. (Eds.), Mineral Nutrition and Plant Disease. APS Press,St. Paul, MN, pp. 177–188, Chapter 12.

AO, 1994. Water quality for agriculture. In: FAO Irrigation and DrainagePapers, Retrieved on January 10, 2013 at: http://www.fao.org/docrep/003/T0234E/T0234E01.htm#ch1

aust, S.D., Aly, O.M., 1983. Chemistry of Water Treatments. Butterworth Publishers,Woburn, MA, pp. 723.

eder, G., Umali, D.L., 1993. The adoption of agricultural innovations. Technol. Fore-cast. Soc. 43, 215–239.

isher, P.R., Huang, J., Looper, A., Minsk, D., Argo, W.R., Vetanovetz, R., Zheng, Y., July2008. Water sanitation using chlorine. Greenhouse Manage. Prod. 28 (7), 15–22.

isher, P.R., Argo, W.R., Hong, C., Huang, J., Looper, A., Wiegers, D., Vetanovetz, R.,Zheng, Y., June 2008. Using sodium and calcium hypochlorite for water treat-ment. Greenhouse Manage. Prod. 28 (6), 21–25.

isher, P.R., Argo, W.R., Huang, J., Konjoian, P., Majka, J.M., Marohn, L., Miller, A., Wick,R., Yates, R., September 2008. Chlorine dioxide can treat water. GreenhouseManage. Prod. 28 (9), 14–17.

isher, P., Mohammad-Pour, G., Haskell, D.W., Huang, J., Meador, D., 2013. Water san-itizing agents such as chlorine and chlorine dioxide interact with peat substrateand suspended solids. Acta Hortic. 1013, 279–284.

lemming, C.A., Trevors, J.T., 1989. Copper toxicity and chemistry in the environ-ment: a review. Water Air Soil Pollut. 44, 146–158.

alvis, G., 2002. Chapter 12 Water treatment in: Small Community Water Sup-ply: Technology, People and Partnership. IRC International Water and SanitationCentre, The Netherlands, pp. 266–284.

ergerich, R.C., Dolja, V.V., 2006. Introduction to Plant Viruses, the Invisible Foe. ThePlant Health Instructor., http://dx.doi.org/10.1094/PHI-I-2006-0414-01.

evens, A.J., Donahoo, R.S., Lamour, K.H., Hausbeck, M.K., 2007. Characterization ofPhytophthora capsici from Michigan surface irrigation water. Phytopathology 97(4), 421–428.

ilbert, R.G., Nakayama, F.S., Bucks, D.A., French, O.F., Adamson, K.C., 1981. Trickleirrigation: emitter clogging and other flow problems. Agric. Water Manage. 3(3), 159–178.

imbel, R., Graham, N.J.D., Collins, M.R., 2007. Recent Progress in Slow Sand andAlternative Biofiltration Processes. IWA Publishing, London, pp. 574.

oldberg, N.P., Stanghellini, M.E., Rasmussen, S.L., 1992. Filtration as a method forcontrolling Pythium root rot of hydroponically grown cucumbers. Plant Dis. 76(8), 777–779.

racia-Garza, J.A., Allen, W., Blom, T.J., Brown, W., 2002. Pre- and post-plant applica-tions of copper-based compounds to control Erwinia soft rot of calla lilies. Can.J. Plant Pathol. 24 (3), 274–280.

raham, T., Zhang, P., Zheng, Y., Dixon, M.A., 2009. Phytotoxicity of aqueous ozoneon five container-grown nursery species. HortScience 44 (3), 774–780.

raham, T., Zhang, P., Dixon, M., 2011. Aqueous ozone in the root zone: friend orfoe? J. Hortic. For. 3 (2), 58–62.

raham, T., Zhang, P., Woyzbun, E., Dixon, M., 2011b. Response of hydroponic tomatoto daily applications of aqueous ozone via drip irrigation. Sci. Hortic. 129 (3),464–471.

ranke, L.L., Hausbeck, M.K., 2010. Effects of temperature, concentration, age, andalgaecides on Phytophthora capsici zoospore infectivity. Plant Dis. 94 (1), 54–60.

r Management 143 (2014) 9–28

Grech, N.M., Rijkenberg, F.H.J., 1991. Injection of electrolytically generated chlorineinto citrus microirrigation systems for the control of certain waterborne rootpathogens. Plant Dis. 76 (5), 457–546.

Hallidri, M., 2004. Effect of silver nitrate on induction of staminate flowers in gynoe-cious cucumber line (Cucumis sativus L.). Acta Hortic. 637, 149–154.

Hardham, A., 2001. The cell biology behind Phytophthora pathogenicity. Austral.Plant Pathol. 30 (2), 91–98.

Havelaar, A.H., 1994. Application of HACCP to drinking water supply. Food Control5 (3), 145–152.

Hayes, C., Evans, L., Fisher, P.R., Frances, A., Vetanovetz, R., Zheng, Y., January 2009.Combat pathogens, algae, with ozone treatment. Greenhouse Manage. Prod. 29(1), 16–20.

Headley, T., Dirou, J., Huett, D., Stovold, G., Davison, L., 2005. Reed beds for the reme-diation and recycling of nursery runoff water. Austral. J. Environ. Manage. 12 (1),27–36.

Helbling, D.E., VanBriesen, J.M., 2007. Free chlorine demand and cell survival ofmicrobial suspensions. Water Res. 41 (19), 4424–4434.

Hijnen, W.A.M., Beerendonk, E.F., Medema, G.J., 2006. Inactivation credit of UV radi-ation for viruses, bacteria and protozoan (oo) cysts in water: a review. WaterRes. 40 (1), 3–22.

Hill, S.A., Miyasaka, S.C., Yost, R.S., 2000. Taro responses to excess copper in solutionculture. HortScience 35 (5), 863–867.

Hoigné, J., Bader, H., 1976. The role of hydroxyl radical reactions in ozonation pro-cesses in aqueous solutions. Water Res. 10 (5), 377–386.

Hong, C.X., Moorman, G.W., 2005. Plant pathogens in irrigation water: challengesand opportunities. Crit. Rev. Plant Sci. 24 (3), 189–208.

Hong, C.X., Richardson, P.A., 2004. Efficacy of chlorine on Pythium species in irrigationwater. SNA Res. Conf. Proc. 49, 265–267.

Hong, C.X., Richardson, P.A., Kong, P., Bush, E.A., 2003. Efficacy of chlorine on multiplespecies of Phytophthora in recycled nursery irrigation water. Plant Dis. 87 (10),1183–1189.

Hong, C.X., Lea-Cox, J.D., Ross, D.S., Moorman, G.W., Richardson, P.A., Ghimire, S.R.,Kong, P., 2009. Containment basin water quality fluctuation and implicationsfor crop health management. Irrig. Sci. 27 (6), 485–496.

Hopkins, D.L., Thompson, C.M., Lovic, B., 2009. Management of transplant housespread of Acidovorax avenae subsp. citrulli on cucurbits with bactericidal chem-icals in irrigation water. Online Plant Health Prog., http://dx.doi.org/10.1094/PHP-2009-0129-01-RS.

Huang, J., Meador, D.P., Fisher, P.R., Decio, D.B., Horner, W.E., 2011. Disinfestantchemicals to control waterborne pathogens are deactivated by peat particlesin irrigation water. Proc. Fla. State Hortic. Soc. 124, 289–293.

Huett, D.O., 2002. Constructed Wetlands to Reduce Nutrient and Pathogen Loads inRecycled Nursery Water, Horticulture Australia Final Report NY98008., pp. 113.

Hyder, N., Coffey, M.D., Stanghellini, M.E., 2009. Viability of oomycete propagulesfollowing ingestion and excretion by fungus gnats, shore flies, and snails. PlantDis. 93, 720–726.

Igura, N., Fujii, M., Shimoda, M., Hayakawa, I., 2004. Research note: inactivationefficiency of ozonated water for Fusarium oxysporum conidia under hydroponicgreenhouse conditions. Ozone: Sci. Eng. 26, 517–521.

James, E., Mebalds, M., Beardsell, D., van der Linden, A., Tregea, W., 1996.Development of Recycled Water Systems for Australian Nurseries. Hor-ticultural Research and Development Corporation, Final report NY320.Retrieved on January 10, 2013 from: http://www.ngia.com.au/Story?Action=View&Story id=1751

Jarvis, R., 1992. Managing Diseases in Greenhouse Crops. APS Press, St. Paul, MN, pp.288.

Juanico, M., Azov, Y., Teltsch, B., Shelef, G., 1995. Effect of effluent addition to afreshwater reservoir on the filter clogging capacity of irrigation water. WaterRes. 29 (7), 1695–1702.

Junli, H., Li, W., Nenqi, R., Li, L.X., Fun, S.R., Guanle, Y., 1997. Disinfection effect ofchlorine dioxide on viruses, algae and animal planktons in water. Water Res. 31(3), 455–460.

Karakaya, D., Padem, H., 2012. Effects of silver nitrate applications on cucumbers(Cucumis sativus L.) morphology. Afr. J. Biotechnol. 11 (72), 13664–13669.

Kobayashi, F., Ikeura, H., Ohsato, S., Goto, T., Tamaki, M., 2011. Disinfection usingozone microbubbles to inactivate Fusarium oxysporum f. sp. melonis and Pecto-bacterium carotovorum subsp. carotovorum. Crop Prot. 30 (11), 1514–1518.

Krauthausen, H.J., Laun, N., Wohanka, W., 2011. Methods to reduce the spread of theblack rot pathogen, Xanthomonas campestris pv. campestris, in brassica trans-plants. J. Plant Dis. Prot. 1 (118), 7–16.

Kuhns, L.J., Sydnor, T.D., 1976. Copper toxicity in woody ornamentals. J. Arboricult.2, 68–72.

Lane, V., 2004. Audit and Gap Analysis of Nursery Waste-water Research and Com-munication. Horticultural Australia Ltd, Sydney, Australia, Retrieved on January10, 2013 from: http://www.ngia.com.au/Story?Action=View&Story id=1849

Lang, J.M., Rebits, B., Newman, S.E., Tisserat, N., 2008. Monitoring mortality ofPythium zoospores in chlorinated water using oxidation reduction potential.Online Plant Health Prog., http://dx.doi.org/10.1094/PHP-2008-0922-01-RS.

LeChevallier, M.W., Cawthon, C.D., Lee, R.G., 1988. Inactivation of biofilm bacteria.Appl. Environ. Microbiol. 54 (10), 2492–2499.

Lee, E., Oki, L., 2013. Slow sand filters effectively reduced Phytophthora after a
pathogen switch from Fusarium and simulated pump failure. Water Res. 47,5121–5129.
Levine, A.D., Tchobanoglous, G., Asano, T., 1985. Characterization of the size distribu-tion of contaminants in wastewater: treatment and reuse implications. J. WaterPollut. Control Federation 57 (7), 805–816.























































































































































































































































































http://www.fao.org/docrep/003/T0234E/T0234E01.htm

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dx.doi.org/10.1094/PHI-I-2006-0414-01



































































































































































































































































































































































































































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R.E. Raudales et al. / Agricultural

ewis Ivey, M.L., Miller, S.A., 2013. Assessing the efficacy of pre-harvest, chlorine-based sanitizers against human pathogen indicator microorganisms andPhytophthora capsici in non-recycled surface irrigation water. Water Res. 47,4639–4651.

in, Y.E., Stout, J.E., Yu, V.L., 2011. Controlling Legionella in hospital drinking water:an evidence-based review of disinfection methods. Infect. Control Hosp. Epi-demiol. 32 (2), 166–173.

oo, S.L., Fane, A.G., Krantz, W.B., Lim, T.T., 2012. Emergency water supply: a reviewof potential technologies and selection criteria. Water Res. 46 (10), 3125–3151.

achado, P.D.S., Alfenas, A.C., Coutinho, M.M., Silva, C.M., Mounteer, A.H., Maf-fia, L.A., Freitas, C.D.S., 2013. Eradication of plant pathogens in forest nurseryirrigation water. Plant Dis. 97 (6), 780–788.

aier, R.M., Pepper, I.L., Gerba, C.P., 2009. Environmental Microbiology, 2nd ed.Elsevier Academic Press, Burlington, MA, pp. 598.

angiafico, S.S., Newman, J.P., Mochizuki, M.J., Zurawski, D., 2008. Adoption of sus-tainable practices to protect and conserve water resources in container nurserieswith greenhouse facilities. Acta Hortic. 797, 367–372.

arra, M., Pannell, D.J., Abadi Ghadim, A., 2003. The economics of risk, uncertaintyand learning in the adoption of new agricultural technologies: where are we onthe learning curve? Agric. Syst. 75 (2), 215–234.

arschner, H., 1995. Mineral Nutrition. Academic Press, London, pp. 889.cPherson, L.L., 1993. Understanding ORP’s Role in the Disinfection Process. Tech-

nology Trends for Water/wastewater Industry Leaders, Retrieved on August28 2012 from: http://www.gfsignet.com/go/?action=GF DocumentDownload&doc uuid=4A78AA2919993E1D34843FFD3F151AB1

eador, D.P., Fisher, P.R., 2013. Ammonium in nutrient solutions decrease free chlo-rine concentration from sodium hypochlorite. HortScience 48 (10), 1304–1308.

eador, D.P., Fisher, P.R., Harmon, P.F., Peres, N.A., Teplitski, M., Guy, C.L., 2012.Survey of physical, chemical, and microbial water quality in greenhouse andnursery irrigation water. HortTechnology 22 (6), 778–786.

eador, D.P., Fisher, P.R., Teplitski, M., 2013. The use of petrifilms to quantify aer-obic bacteria in irrigation water. Proc. Fla. State Hort. Soc. 2012 125, 340–342.

ebalds, M., Hepworth, A.G., van der Linden, A., Beardsell, D., 1995. Disinfestationof plant pathogens in recycled water using uv radiation and chlorine dioxide. In:Development of Recycled Water Systems for Australian Nurseries, HRDC FinalReport No. NY320.

ebalds, M., van der Linden, A., Bankier, M., Beardsell, D., 1996. Using Ultra VioletRadiation and Chlorine Dioxide to Control Fungal Plant Pathogens in Water, TheNursery Papers 1996–2005., pp. 1–2.

iller, L.P., McCallan, S.E.A., 1957. Toxic action of metal ions to fungus spores. Agric.Food Chem. 5 (2), 116–122.

inuto, A., Gaggero, L., Gullino, M.L., Garibaldi, A., 2008. Influence of pH, nutri-ent solution disinfestation and antagonists application in a closed soillesssystem on severity of Fusarium wilt of Gerbera. Phytoparasitica 36 (3), 294–303.

oens, M., Hendrickx, G., 1992. Drain water filtration for the control of nematodesin hydroponic-type systems. Crop Prot. 11 (1), 69–73.

ohammad-Pour, G., Haskell, D.W., Huang, J., Fisher, P.R., 2011. Efficacy of coppersanitizers in subirrigation tanks. Proc. Fla. State Hortic. Soc. 124, 281–284.

orris, J.C., 1966. The acid ionizations constant of HOCl from 5 to 35◦ . J. Phys. Chem.70 (12), 3798–3805.

edderhoff, E., 2000. Hydrogen peroxide for cleaning irrigation system in: pathogencontrol in soilless cultures. Commercial Grower 55 (10), 32–34.

ewman, S., 2004. Disinfecting irrigation water for disease management. In: 20thAnnual Conference on Pest Management of Ornamentals Society of AmericanFlorists, San Jose, February, 20–22, 2004, pp. 1–10.

ielsen, C.J., Ferrin, D.M., Stanghellini, M.E., 2006. Efficacy of biosurfactants in themanagement of Phytophthora capsici on pepper in recirculating hydroponic sys-tems. Can. J. Plant. Pathol. 28, 450–460.

breza, T., Clark, M., Boman, B., Borisova, T., Cohen, M., Dukes, M., Frazer, T., Hanlon,E., Havens, K., Martinez, C., Migliaccio, K., Shukla, S., Wright, A., 2010. A guide toenvironmental protection agencies numeric nutrient water quality criteria forFlorida. Univ. Fla. Inst. Food Agr. Sci. Res. Bull., SL-316.

hashi-Kaneko, K., Yoshii, M., Isobe, T., Park, J.S., Kurata, K., Fujiwara, K., 2009. Nutri-ent solution prepared with ozonated water does not damage early growth ofhydroponically grown tomatoes. Ozone: Sci. Eng. 31 (1), 21–27.

htani, T., Kaneko, A., Fukuda, N., Hagiwara, S., Sase, S., 2000. Development of amembrane disinfection system for closed hydroponics in a greenhouse. J. Agric.Eng. Res. 77 (2), 227–232.

agliaccia, D., Ferrin, D., Stanghellini, M.E., 2007. Chemo-biological suppression ofroot infecting zoosporic pathogens in recirculating hydroponic systems. PlantSoil 299 (1–2), 163–179.

arke, J.L., Grünwald, N.J., 2012. A systems approach for management of pests andpathogens of nursery crops. Plant Dis. 96 (9), 1236–1244.

erez Cachafeiro, S., Mato Naveira, I., González García, I., 2007. Is copper–silverionisation safe and effective in controlling legionella? J. Hosp. Infect. 67 (3),209–216.

eterson, P., 2001. Biological Soil Crusts: Ecology and Management. Bureau of Lan-guage Management Technical Reference, pp. 1730–1732.

ettitt, T., 2003. Fertigation: developments in pathogen removal from recycled
water. In: Proceedings-International Fertiliser Society, IFS, 1999, pp. 1–20.
oncet, C., Offroy, M., Bonnet, G., Brun, R., 2001. Disinfection of recycling water inrose cultures. Acta Hortic. 547, 121–127.

orter, L.D., Johnson, D.A., 2004. Survival of Phytophthora infestans in surface water.Phytopathology 94 (4), 380–387.

r Management 143 (2014) 9–28 27

Pottorff, L.P., Panter, K.L., 1997. Survey of Pythium and Phytophthora spp. inirrigation water used by Colorado commercial greenhouses. HortTechnology 7(2), 153–155.

Qiang, Z., Adams, C.D., 2004. Determination of monochloramine formation rateconstants with stopped-flow spectrophotometry. Environ. Sci. Technol. 3,1435–1444.

Raudales, R., (Ph.D. thesis) 2013. Characterization of Water Treatment Technologiesin Irrigation. University of Florida.

Rav-Acha, C.H., Kummel, M., Salamon, I., Adin, A., 1995. The effect of chemical oxi-dants on effluent constituents for drip irrigation. Water Res. 29 (1), 119–129.

Raviv, M., Lieth, J.H., 2007. Soilless Culture: Theory and Practice. Boston, Elsevier,pp. 587.

Rens, L.R., (Master thesis) 2011. Chlorine Dioxide as Sanitizing Agent inRecirculating Irrigation for Greenhouse Hydroponic Bell Peppers. Univer-sity of Florida, Retrieved on January 10, 2013 from: http://etd.fcla.edu/UF/UFE0043811/DAVIES L.pdf

Ristaino, J.B., Gumpertz, M.L., 2000. New frontiers in the study of dispersal and spatialanalysis of epidemics caused by species in the genus Phytophthora. Annu. Rev.Phytopathol. 38 (1), 541–576.

Robbs, P.G., Bartz, J.A., Brecht, J.K., Sargent, S.A., 1995. Oxidation–reduction potentialof chlorine solutions and their toxicity to Erwinia carotovora subsp. carotovoraand Geotrichum candidum. Plant Dis. 79 (2), 158–162.

Roberts, P.D., Muchovej, R.M., 2009. Evaluation of Tailwater from Vegetable Fieldsfor Recovery of Phytopathogens and Methods to Reduce Contamination (B201),Southwest Florida Water Management District Report.

Rogers, E.M., 2003. Diffusion of Innovations, 5th ed. Free Press, NY.Rogers, D.H., Lamm, F.R., Alam, M., 2003. Subsurface drip irrigation systems water

quality assessment guidelines. In: Irrigation management Series, Kansas StateUniversity Agricultural Experimental Station and Cooperative Extension Service,Research Bulletin MF-2575.

Rohr, U., Senger, M., Selenka, F., Turley, R., Wilhelm, M., 1999. Four years ofexperience with silver–copper ionization for control of Legionella in a Ger-man University Hospital hot water plumbing system. Clin. Infect. Dis. 29 (6),1507–1511.

Rosner, A., Lachman, O., Pearlsman, M., Feigelson, L., Maslenin, L., Antignus, Y., 2006.Characterisation of cucumber leaf spot virus isolated from recycled irrigationwater of soil-less cucumber cultures. Ann. Appl. Biol. 149 (3), 313–316.

Runia, W.Th., 1994a. Disinfection of recirculation water from closed cultivation sys-tems with ozone. Acta Hortic. 361, 388–396.

Runia, W.Th., 1994b. Elimination of root infecting pathogens in recirculation waterfrom closed cultivation systems by ultra-violet radiation. Acta Hortic. 361,361–371.

Runia, W.Th., 1995. A review of possibilities for disinfection of recirculation waterfrom soilless cultures. Acta Hortic. 382, 221–229.

Runia, W.Th., Amsing, J.J., 2001. Lethal temperatures of soilborne pathogens in recir-culation water from closed cultivation systems. Acta Hortic. 554, 333–339.

Schuerger, A.C., Hammer, W., 2009. Use of cross-flow membrane filtration in arecirculating hydroponic system to suppress root disease in pepper caused byPythium myriotylum. Phytopathology 99 (5), 597–607.

Schwarz, D., Gross, W., 2004. Algae affecting lettuce growth in hydroponic systems.J. Hort. Sci. Biotechnol. 79 (4), 554–559.

Schwarz, D., Krienitz, L., 2005. Do algae cause growth-promoting effects onvegetables grown hydroponically? In: IPI–NATESC-CAU-CAAS InternationalSymposium on Fertirrigation, September 01, 2005, Beijing, China.

Slade, S.J., Pegg, G.F., 1993. The effect of silver and other metal ions on the in vitrogrowth of root-rotting Phytophthora and other fungal species. Ann. Appl. Biol.122, 233–251.

Stanghellini, M.E., Miller, R.M., 1997. Biosurfactants: their identity and potentialefficacy in the biological control of zoosporic plant pathogens. Plant Dis. 81 (1),4–12.

Stanghellini, M.E., Stowell, L.J., Bates, M.L., 1984. Control of root rot of spinach causedby Pythium aphanidermatum in a recirculating hydroponic system by ultravioletirradiation. Plant Dis. 68 (12), 1075–1076.

Stanton, J.M., O’Donnell, W.E., 1994. Hatching, motility, and infectivity of root-knotnematode (Meloidogyne javanica) following exposure to sodium hypochlorite.Aus. J. Exp. Agric. 34, 105–108.

Steddom, K., Pruett, J., Unpublished Research Report 2012. Efficacy of sanitizers onwater samples from greenhouse and nursery operations with natural popula-tions of Pythiacious species. Texas AgriLife Extension Service, Department ofPlant Pathology and Microbiology, Overton, TX.

Stewart-Wade, S.M., 2011. Plant pathogens in recycled irrigation water in commer-cial plant nurseries and greenhouses: their detection and management. Irrig.Sci. 29 (4), 267–297.

Stout, J.E., 2003. Experiences of the first 16 hospitals using copper–silver ioniza-tion for Legionella control: implications for the evaluation of other disinfectionmodalities. Infect. Control Hosp. Epidemiol. 24 (8), 563–568.

Suidan, M.T., Cross, W.H., Chacey, K.A., 1980. Extended dechlorination studies withgranular activated carbon filters. J. Water Pollut. Control Federation 52 (11),2634–2646.

Suslow, T.V., 2004. Oxidation–Reduction Potential (ORP) for Water Disinfec-tion Monitoring, Control and Documentation. Publication 8149. Univer-
sity of California, Retrieved on August 28, 2012 from: http://anrcatalog.ucdavis.edu/pdf/8149.pdf
Sutton, J.C., Yu, H., Grodzinski, B., Johnstone, M., 2009. Relationships of ultravioletradiation dose and inactivation of pathogen propagules in water and hydroponicnutrient solutions. Can. J. Plant. Pathol. 22 (3), 300–309.

























































































































































http://www.gfsignet.com/go/?action=GF_DocumentDownload&doc_uuid=4A78AA2919993E1D34843FFD3F151AB1

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achikawa, M., Yamanaka, K., Nakamuro, K., 2009. Studies on the disinfection andremoval of biofilms by ozone water using an artificial microbial biofilm system.Ozone: Sci. Eng. 31 (1), 3–9.

hompson, D.L., 1965. Control of bacterial stalk rot of corn by chlorination of waterin sprinkler irrigation. Crop Sci. 5 (4), 369–370.

hurman, R.B., Gerba, C.P., Bitton, G., 2009. The molecular mechanisms of copper andsilver ion disinfection of bacteria and viruses. Crit. Rev. Environ. Sci. Technol. 18(4), 295–315.

oppe, B., Thinggaard, K., 1998. Prevention of Phytophthora root rot in gerbera byincreasing copper ion concentration in the nutrient solution. Eur. J. Plant Pathol.104 (4), 359–366.

oppe, B., Thinggaard, K., 2000. Influence of copper ion concentration and electricalconductivity of the nutrient solution on Phytophthora cinnamomi in ivy grownin ebb and flow systems. J. Phytopathol. 148 (11–12), 579–585.

oussoun, T.A., Nelson, P.E., 1976. A Pictorial Guide to the Identification of FusariumSpecies, 2nd ed. Pennsylvania State University Press, University Park, PA, pp. 43.

u, C., Hardwood, B., 2005. Disinfestation of recirculating nutrient solution by fil-tration as a means to control Pythium root rot of tomatoes. Acta Hortic. 695,303–308.

u, J.C., Zhang, W.Z., 2000. Comparison of heat, sonication and ultraviolet irradia-tion in eliminating Pythium aphanidermatum zoospores in recirculating nutrientsolution. Acta Hortic. 532, 137–142.

fer, T., Werres, S., Posner, M., Wessels, H.P., 2008. Filtration to eliminate Phytoph-thora spp. from recirculating water systems in commercial nurseries. OnlinePlant Health Prog., http://dx.doi.org/10.1094/PHP-2008-0314-01-RS.

S-EPA, 1999. Alternative Disinfectants and Oxidants Guidance Manual, EPA 815-R-99-014, Washington, DC.

S-EPA, 2000. Toxicological Review of Chlorine Dioxide and Chlorite, EPA-635-R-00-007, Washington, DC.

S-EPA, 2005. Membrane Filtration Guidance Manual, EPA 815-R-06-009, Washing-ton, DC.

S-EPA, 2009. Bromine summary document: registration review preliminary workplan. In: Prevention Pesticides and Toxic Substances, EPA-HQ-OPP-2009-0167,Washington, DC.

S-EPA, 2013a. Water Basic Information about Regulated Drinking Water Con-taminants, Retrieved on May 16, 2013 from: http://water.epa.gov/drink/contaminants/basicinformation/copper.cfm

S-EPA, 2013b. Rhamnolipid Biosurfactant, Factsheet 110029, Washington, DC.S-FDA, 2013. Food Safety Modernization Act, Washington, DC.an der Bruggen, B., Vandecasteele, C., Van Gestel, T., Doyen, W., Leysen, R., 2003.

A review of pressure-driven membrane processes in wastewater treatment anddrinking water production. Environ. Prog. 22 (1), 46–56.

an Os, E.A., 2010. Disease management in soilless culture systems. Acta Hortic. 883,385–394.

an Os, E.A., Amsing, J.J., van Kuik, A.J., Willers, H., 1999. Slow sand filtration: a poten-tial method for the elimination of pathogens and nematodes in recirculatingnutrient solutions from glasshouse-grown crops. Acta Hortic. 481, 519–526.

an Wyk, S.J., Boutigny, A.L., Coutinho, T.A., Viljoen, A., 2012. Sanitation of a SouthAfrican forestry nursery contaminated with Fusarium circinatum using hydro-gen peroxide at specific oxidation reduction potentials. Plant Dis. 96 (6), 875–880.

anachter, A., Thys, L., Van Wambeke, E., Van Assche, C., 1988. Possible use of ozonefor disinfestation of plant nutrient solutions. Acta Hortic. 221, 295–302.

änninen, I., Koskula, H., 1998. Effect of hydrogen peroxide on algal growth, cucum-ber seedlings and the reproduction of shoreflies (Scatella stagnalis) in rockwool.Crop Prot. 17 (6), 547–553.

iera, M.J., Melo, L.F., Pinheiro, M.M., 1993. Biofilm formation: hydronamic effectson internal diffusion and structure. Biofouling 7 (1), 67–80.

r Management 143 (2014) 9–28

Vymazal, J., 2005. Horizontal sub-surface flow and hybrid constructed wetlandssystems for wastewater treatment. Ecol. Eng. 25, 478–490.

Vymazal, J., 2009. The use constructed wetlands with horizontal sub-surface flowfor various types of wastewater. Ecol. Eng. 35 (1), 1–17.

Weil, I., Morris, J.C., 1949. Kinetic studies on the chloramines. I. The rates of formationof monochloramines, N-chlormethylamine and N-chlordimethylamine. J. Am.Chem. Soc. 71 (5), 1664–1671.

Weller, D.M., Raaijmakers, J.M., McSpadden Gardener, B.B., Thomashow, L.S.,2002. Microbial populations responsible for specific suppressiveness to plantpathogens. Annu. Rev. Phytopathol. 40, 309–348.

White, G.C., 1992. Handbook of Chlorination and Alternative Disinfectants, vol.1308., third ed. Van Nostrand, NY.

White, S.A., Taylor, M.D., Polomski, R.F., Albano, J.P., 2011. Constructed Wetlands: AHow to Guide for Nurseries, Retrieved on August 01, 2013 from: http://www.clemson.edu/extension/horticulture/nursery/images/cws howtoguide small.pdf

Wohanka, W., 1995. Disinfection of recirculating nutrient solutions by slow sandfiltration. Acta Hortic. 382, 246–255.

Wohanka, W., Fehres, H., 2006a. Efficacy of Water Treatment with the Aquahort®

– System Against Fusarium oxysporum f. sp. Cyclaminis. Geisenheim ResearchCenter, Dpt. Phytomedicine, Germany.

Wohanka, W., Fehres, H., 2006b. Efficacy of Water Treatment with the Aquahort®

– System Against Pythium aphanidermatum. Geisenheim Research Center, Dpt.Phytomedicine, Germany.

Wohanka, W., Fehres, H., 2006c. Efficacy of Water Treatment with the Aquahort®

– System Against Xanthomonas hortorum pv. pelargonii. Geisenheim ResearchCenter, Dpt. Phytomedicine, Germany.

Wohanka, W., Fehres, H., 2007a. Efficacy of Water Treatment with the Aquahort®

– System Against Clavibacter michiganensis ssp. michiganensis. GeisenheimResearch Center, Dpt. Phytomedicine, Germany.

Wohanka, W., Fehres, H., 2007b. Efficacy of Water Treatment with the Aquahort®

– System Against Ralstonia solanacearum Race 3. Geisenheim Research Center,Dpt. Phytomedicine, Germany.

Wohanka, W., Luedtke, H., Ahlers, H., Luebke, M., 1999. Optimization of slow sand fil-tration as a means for disinfecting nutrient solutions. Acta Hortic. 481, 539–544.

Wohanka, W., Becker, D., Fehres, H., 2006. Efficacy of Water Treatment with theAquahort® – System Against Agrobacterium tumefaciens. Geisenheim ResearchCenter, Dpt. Phytomedicine, Germany.

Wohanka, W., Fehres, H., Schoenbach, W., 2007. Efficacy of Water Treatment withthe Aquahort® – System Against Erwinia carotovora spp. carotovora. GeisenheimResearch Center, Dpt. Phytomedicine, Germany.

Wohanka, W., Becker, D., Fehres, H., 2009. Efficacy of Water Treatment with theAquahort® – System Against Trichoderma asperellum. Geisenheim Research Cen-ter, Dpt. Phytomedicine, Germany.

Wolfe, R.L., 1990. Ultraviolet disinfection of potable water. Environ. Sci. Technol. 24(6), 768–773.

Yan, D., Bai, Z., Rowan, M., Gu, L., Shumei, R., Yang, P., 2009. Biofilm structure and itsinfluence on clogging in drip irrigation emitters distributing reclaimed waste-water. J. Environ. Sci. 21 (6), 834–841.

Yao, K.S., Hsieh, Y.H., Chang, Y.J., Chang, C.Y., Cheng, T.C., Liao, H.L., 2010. Inactiva-tion effect of chlorine dioxide on phytopathogenic bacteria in irrigation water.J. Environ. Eng. Manage. 20 (3), 157–160.

Yiaosumi, W., Evans, L., Rogers, L., 2005. Farm Water Quality and Treatment, Ag Facts
AC 2, 9th ed. Department of Primary Industries Australia Government, Australia.
Zheng, Y., Wang, L., Dixon, M., 2005. Greenhouse pepper growth and yield responseto copper application. HortScience 40 (7), 2132–2134.

Zhou, H., Smith, D.W., 2002. Advanced technologies in water and wastewater treat-ment. J. Environ. Eng. Sci. 1 (4), 247–264.


































































































































































































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